232 Chapter 8 with the “macroevolutionary” processes of speciation and extinction. Yet we will show that a deep understanding of these processes also requires a microevolutionary perspective on how populations respond to environmental change in both space and time. Speciation ‘Mechanisms of Genetic Differentiation Speciation is a branching process in which different kinds of organisms origi- nate from a single ancestral population. The magnitude of this process is stag- gering when we consider that all species of green land plants that have ever lived ultimately share a common ancestor in a simple green alga that lived 500 million years ago, that all vertebrates are traceable to some ancient chordate, and that millions of species of insects have evolved in the 400 million years since their ancestor first invaded land. Most of the species in all of these lin- eages are no longer around; they lived in the past and went extinct. How did this diversity come to be? Genetic drift. Populations diverge (or converge) in their genetic characteris- tics as a result of the microevolutionary forces of mutation, genetic drift, gene flow, and natural selection. Different forms of a gene at the same locus, known as alleles, are responsible for differences among individuals in their heritable traits, New alleles arise by mutation, and changes in the frequencies of alleles in populations occur primarily through genetic drift, natural selection, and gene flow. Genetic drift is a relatively weak force because it involves changes in the genetic constitution of a population caused solely by chance. Given suf- ficient time—which usually means many generations—the frequencies of alle- les in a population tend to change randomly as different individuals happen to survive, mate, and produce offspring. Genetic drift has relatively little effect in large populations, but can have important influences on the evolution of small populations. How small is small is a matter of considerable discussion in evolutionary biology. Nevertheless, if new species start from small founding populations, as many island forms undoubtedly do, then genetic drift may play an important role in their initial differentiation, as we shall see below. Natural selection. Natural selection, on the other hand, can be a potent force for evolutionary change in both large and small populations. Natural selection is the change in a population that occurs because individuals express genetic traits that alter their interactions with their environment so as to enhance their survival and reproduction. Over many generations, alleles for such adaptive traits tend to increase in frequency at the expense of alleles that confer less fitness. Populations tend to diverge if there is sufficient variation in the environment to select for different characteristics to deal with different ‘environmental conditions. This fine-tuning of phenotypes to environmental heterogeneity can be readily documented. Above we mentioned industrial melanism. Within the last 150 years, moths in industrialized areas around cities have evolved dark color patterns to match their sooty backgrounds and are thus less visible to their avian predators (Kettlewell 1961). Rapid evolution by natural selection has also occurred in house sparrows. Since being introduced to North Amer- ica from Europe less than 200 years ago, these enormously successful birds have not only spread to colonize most of the continent, but have also evolved distinct geographic races Johnston and Sealander 1964, 1971; Johnston et al. 1973; Johnston 1977). This variation, in characteristics such as body size, colorpattern, and physiological characteristics, is similar to that seen in the deer mouse (see Figure 8.5); it reflects different adaptations to different environ ‘mental conditions, Gene flow. Migration, or gene flow, already mentioned in Chapter 4, often tends to act counter to genetic drift and natural selection to retard genetic divergence. Individuals thet migrate to a new area carry their genes with them, and if they subsequently reproduce successfully, they inject their genes into the local population. Such migration, therefore, tends to have a homoge- nizing influence, preventing or at least retarding the development of geo- ‘graphically isolated and genetically differentiated populations. Geographic variation. There is often a geographic component to genetic divergence, because both genetic drift and natural selection are facilitated, and ‘gene flow is retarded, by geographic isolation. Genetic drift can be an impor- tant force in small, isolated populations, such as those that inhabit small out- lying patches at the periphery of a species range, or those that have recently been founded by long-distance colonization. A population started by only a few colonizing individuals contains only a small random sample of the alleles present in the ancestral population. The genetic drift that occurs in these cir- cumstances has been termed the founder effect. Mayr (1942) suggested that this process accounts for the apparently random differences often found among the bird populations on different islands (Figure 8.4), each of which ‘was probably derived from a few successful colonists. Experimental evidence suggests that the founder effect can play a major role in speciation, because this initially random genetic sampling has effects on the subsequent genetic differentiation of small colonizing populations (e.g., Carson and Kaneshiro 1976; Templeton 1980a; Carson 1981). Speciation and Extinction 233 Figure 8.4 Divergence of populations of the Old World flycatcher (Mona sodgsnyile and Crcastonecents) on the Solomon Islands east of New Guinea. These ; seemingly chance diferences among popdlations were interpreted by Mayr (4543) a electing the founder elfet the random sampling of genes Pre Sent inthe ancestral population ie to the small amber of ndividals in a2) @ ‘Ysabel Island New G&rgin ug sand Mala land ‘Guadaleanal Island Bauro itand) the initial colonizing populations. (From Mayr 1942.) @ white Bchertmst MiBlacksae : CQ" Sie yn \ a8 eg Ai iE 4 g2ee Pee BestsGeographic separation of populations also facilitates genetic differentiation by natural selection. Different environmental regimes tend to select for differ- cent traits, and spatially isolated populations are likely to occur in different environments. The effects ofnatural selection caused by spatial environmental heterogeneity are exemplified by data on small mammals. As mentioned in Chapter 4, the coat color of the deer mouse (Peromyscus maniculatus) varies greaily over the wide geographic range of the species (Figure 8.5). The color of the dorsal fur closely matches the color of the soil or other substrate on which the animal is likely to be active, reflecting the consequences of selection by predators. Dice (1947) performed a classic experiment showing that owls selectively captured mice that contrasted with their background. Patterns of geographic variation can take many forms. The term line is used to describe a gradual change in one or more features along a single envi- ronmental gradient. Many birds and mammals exhibit clinal variation in clutch or litter sizes with latitude and elevation (eg,, for Peromyscus see Dun- ‘mire 1960; Lord 1960; Smith and McGinnis 1968; Spencer and Steinhoff 1968) (Figure 8.6). Such variation presumably reflects the adaptation of life history traits to environments that differ in temperature, seasonality, productivity, and other factors. Similarly, clines in physiological characteristics of plants and insects show that populations at progressively higher latitudes are adapted to colder temperature regimes. Allopatric Speciation Perhaps the simplest and most frequent process of speciation is the one that, occurs when populations are geographically isolated, so that gene flow between them is mostly or entirely cut off. This process is termed allopatric speciation, meaning divergence that occurs in different places. The classic model of allopatric speciation by geographic subdivision (also called geo- ‘graphic speciation) was chempioned by Emst Mayr (1942, 1963). © Colorado © California Bs . L . j . Bap ee t *r000 2000 300000020 30 rn EA w Elevation (mn) Latitude (*) Speciation and Extinction 235 Figure 8.6 Latitudinal and eleva- tional variation in average litter size of the deer mouse (Peromryscus manicula- ‘us). Note that the number of young pet litter increases with both latitude and elevation. Presumably, large litters are advantageous in colder climates, perhaps because the shorter growing Seasons favor fewer litters per year ‘with more young per litter (see also Chapter 16)236 Chapter 8 fits environment is heterogeneous, a geographically widespread ancestral population will tend to develop regional genetic differences in response to either natural selection or genetic drift. Because of barriers that limit dispersal, free gene flow from one end of the range to the other rarely occurs. Thus pop- ulations living in environmentally distinct and geographically separated regions tend to become somewhat differentiated from one another, but some gene flow maintains the genetic cohesiveness of the species. The regional races of house sparrows and deer mice, and the clinal variation in litter and clutch sizes mentioned above, are examples of such differentiation, If, however, the regional populations become sufficiently isolated that the cohesive gene flow between them is cut off or drastically reduced, then they ‘become independent evolutionary units. Without dispersal and gene flow, the isolated populations tend to diverge. Divergence proceeds more rapidly when substantially different environments subject the isolates to different selective pressures. For example, Darwin called attention to the morphological differ- ences among the giant tortoises of the Galépagos, which are obviously descended from a common ancestor but presently occur on different islands. On some of the most arid islands, where treelike cacti are abundant, the endemic tortoises have evolved long necks and forelimbs and distinctively shaped shells that allow then to reach up high to feed on these plants. On wet- ter islands, where the tortoises feed mostly on lower vegetation, they have more generalized body forms. Isolation: Vicariant and founder events. We can distinguish, at least at the extremes, two ways in which such isolation can occur. At one extreme, some environmental change can create a barrier to dispersal, isolating previously connected and interbreeding populations. Rising sea levels, for example, can isolate an island on a continental shelf, tectonic events can cause part of a con- ‘nent to split off and drift away, or, conversely, landmasses can drift together to isolate formerly continuous oceans. Such changes are called vicariant events, and they usually isolate relatively large populations (Figure 7A). At the other extreme, individuals may disperse across an existing barrier to colo- nize a previously uninhabited region. Such migrations, called dispersal or founder events, are the way in which oceanic islands and many other isolated patches of habitat come to be colonized. They typically involve a small initial population, sometimes only one or a few individuals (Figure 8.7B). As indi- cated above, the mechanisms and rates of initial genetic divergence may differ depending on the mode of isolation. Genetic drift may play a greater role rel- (A) View (@) Founder event Gap ® @ a Figure 8.7 A schematic representation of two oO ‘modes of allopatric speciation: (A) a vicariant event, in which part of a once widely distrib- ‘uted population becomes isolated due to the formation of a geographic barrier, and (B) a founder event, in which a small number of indi- Viduals disperse to found a new geographically ‘isolated population. In both modes the specia- tion process involves several stages: a single an- cestral population (1) gives rise to two isolated populations (2), the isolates diverge (3), and eventually become sufficiently distinct to be rec- ‘ognized as separate species according to one oF ‘more of the species concepts. LN ne iative to selection, and divergence may be more rapid, at least initially, in founder events than in vicariant events (Carson 1971; Bush 1975; Templeton 19802, 1981). Contact and reinforcement. Once isolates have formed and differentiated, there are several possible outcomes. First, they may come back into contact. This may occur either through the disappearance of a geographic barrier or by dispersal across it. If the populations reestablish contact, there are then three possible outcomes: (1) they may not interbreed, or may fail to produce fertile offspring, in which case reproductive isolation is complete and speciation has occurred; (2) the two populations may interbreed extensively, producing fer- tile fit hybrids, so that the populations merge and their differentiation breaks down; or (3) the two populations may hybridize, but the hybrids may be less fit than the offspring of within-population matings. In this last case, selection favoring those individuals that choose mates from within their own popula- tion may be sufficiently strong, to lead to reproductive isolation and the com- pletion of the speciation process, This process of selection for mechanisms that promote within-population matings is termed reinforcement, and the traits that evolve to enhance reproductive isolation are called isolating mechanisms. A final scenario is one in which the isolated populations never do come into contact. In this case reproductive isolation may take a long tome to develop, and, as mentioned above, the isolates will cause problems for a taxonomist trying to apply the biological species concept and decide whether they should bbe considered different species. While there is broad agreement that speciation can, and often does, occur through geographic isolation, there is much less consensus about the details of the process (see Paterson 1982; Otte and Endler 1989). How much do the mechanisms of speciation vary among different kinds of organisms, and even among different speciation events within lineages of closely related organ- isms? What are the relative frequencies of vicariant and founder events? When vicariant events are involved, how often are the isolates small, peripheral pop- ulations as opposed to large fragments of a once continuous population? How often are the initial isolates composed of only a few individuals, so that they are likely to diverge rapidly due to the founder effect and genetic drift, as, opposed to large populations that are less likely to experience rapid genetic change? How important is gene flow in maintaining cohesion and preventing differentiation among populations? How important is the genetic inertia of large populations and the influence of similar selective environments in retarding divergence? Conversely, what are the roles of genetic isolation and. founder events relative to divergent selective pressures in promoting diver- gence of isolated populations? ‘To what extent is there active selection for “reinforcement” of isolating mechanisms, so that individuals actively avoid interbreeding with members of closely related, coexisting species? To what extent does sexual selection for mates with exaggerated traits facilitate the evolution of reproductive isolation? There is much disagreement among evo- Tutionary and systematic biologists on the answers to these questions. We sus- pect that much of it stems from a well-intentioned but misplaced desire to describe one universal process of speciation. Instead of attempting this, we ‘must recognize the enormous variation in the process due to the special char- acteristics of different kinds of organisms and the different historical and envi- ronmental contexts in which speciation occurs. Examples: Allopatric speciation in the Galépagos archipelago. Despite ‘these uncertainties about the details, there can be little doubt that geographic isolation has been a common mode of speciation in many groups. The giant Speciation and Extinction 237238 Chapter 8 Figure 8.8 Adaptive radia- tion in Galapagos finches, showing the diversity of beak shapes and diets. A single an- cestor, a grassquit, colonized the archipelago. Subsequent al- lopatric speciation events, due to repeated episodes of colo- Gace fnegenen snd 13 ve % species. (Ales Futuyma 195, based on Purves etal. 1997; Grant 1986,) tortoises and finches that Darwin observed in the Galapagos archipelago pro- vide examples of populations in different stages of the process. As we have seen, there are distinctly different populations of tortoises on each of the large islands. These populations have diverged from a single ancestor that originally colonized the archipelago and whose descendants stibsequently dispersed to establish populations on the different islands. However, there are no cases in ‘which two or more forms occur on the same island. Even in the unlikely event that individuals immigrated from another island and were sufficiently differ- entiated so that widespread hybridization did not occur, even the largest islands are probably too small and unproductive to support two species of giant tortoises. On the other hand, in Darwin's finches, the final stages of spe- Ciation are represented. Here again, all the species are believed to be derived from a single ancestral population that colonized the archipelago. In the case Seed eaters Geospiza magivotris -Camarhynchus parvuls Se Camarhynchuspstacula BD 2. aa copia treof the finches, however, after diverging in isolation on different islands or in different habitats, some populations have successfully reinvaded already inhabited areas, so that several species (as many as 10 on certain islands) now coexist. These species have not only evolved specific mating behaviors that prevent interspecific hybridization, but have also diverged in morphology and Dehavior to exploit different ecological niches (Figure 8.8). The process of spe- ciation is an ongoing one, and so there are also documented cases of inter island colonization events and of hybridization between incompletely isolated forms (Grant and Grant 1989, 1992), Sympatric Speciation Although many evolutionary biologists once maintained that speciation in ‘most organisms occurs primarily or solely as a result of geographic isolation, ‘most now accept that speciation can, and often does, occur within spatially contiguous populations. This process is called sympatric speciation, meaning divergence that occurs in the same place. Two mechanisms of sympatric spe- ciation have been proposed. Disruptive selection. If strong selective pressures cause a population to adapt to two or more different environmental regimes or niches, they can pro- gressively pull the population apart and eventually result in speciation. Endler (1977; see also Slatkin 1973; Rosenzweig 1978) suggested that such disruptive selection, acting along an environmental gradient, could gradually sharpen clinal variation until a single ancestral population fragmented into two or more species. Such speciation is often termed parapatric or stasipatric because the diverging populations are geographically distinct, but remain in contact, with each other. ‘Bush (1975), Price (1980), and others have argued that sympatric speciation by disruptive selection may be common in certain groups of phytophagous (herbivorous) insects and animal parasites that are highly specialized for spe- cific host species. Among these organisms, successful colonization of a new kind of host must be a rare event, but when it occurs, the colonists are imme- diately subjected to selection for the ability to survive and reproduce in a dras- tically different environment. Usually this selection pressure is intensified by counterevolution of the host to escape from or reject the parasite. Selection to meet the challenge of a new host could potentially lead to the rapid differen- tiation and speciation of totally sympatric populations, in which the organ- isms are spatially close enough to mate, but do not, often because mating occurs on the host. Chromosomal changes. _Sympatric speciation can also occur through chro- mosomal changes. Chance rearrangements of the genetic material of a parent during meiosis, or of an embryo during fertilization or early development, can sometimes change the number of chromosomes or the sequence of genes on chromosomes. Changes in chromosome number are of two kinds: aneuploidy, in which a single chromosome breaks or fuses with another to change the total number by plus or minus ore; or polyploidy, in which an entire additional set of chromosomes is passed on, changing the number by some multiple (e.g. a doubling or tripling). In otter cases, the chromosome number remains the same, but some of the genetic material is either rearranged within a chromo- some (inversion) or transferred to another chromosome (translocation). In diploid organisms, precise pairing during meiosis of the genes and chro- ‘mosomes inherited from each parent usually is necessary to ensure the trans- mission of a complete set of genes to each gamete, and hence to produce Speciation and Extinction 239240 Chapter 8 viable offspring. Consequently, mutant individuals with new chromosomal arrangements often have impaired fertility when they mate with an individual ‘having the original chromosomal arrangement, and may be able to reproduce only by mating with another individual having the new arrangement. For this reason, it is obviously difficult for a population with a new arrangement to become established. However, once established—especially in a small, iso- lated, inbred population—the new type is genetically isolated from its parental population and can diverge rapidly as a new species. ‘Sympatric speciation by way of polyploidy appears to have occurred fre- quently in some groups of organisms, especially plants (e.g., Stebbins 1971; de Wet 1979; Lewis 1979; Briggs and Walters 1984). There are many doct mented ways in which polyploidy has been achieved in plants, but one such process is considered very common (de Wet 1979). Diploid (2N) organisms have two sets of chromosomes and produce haploid (N) gametes by meiosis. Occasionally, a female gamete is formed without undergoing meiosis, and remains diploid (2N). This unreduced gamete can then fuse with a haploid pollen grain (N) to produce a triploid (3N) plant, which will produce triploid gametes because of complications during meiosis. In the next generation, a triploid female gamete can fuse with a haploid pollen grain to yield a tetraploid (4N) zygote, which can survive and produce fertile offspring from diploid (2N) gametes, either by self-fertilization or by crossing with other rare tetraploids in the population. The resulting tetraploid population is immedi- ately genetically isolated from the diploid population, Polyploidy can occur either within a population, called autopolyploidy, or as a result of hybridization between different but usually closely related pop- ulations or species, called allopolyploidy. Allopolyploidy is thought by many researchers to be more common. Because the chromosomes from different species may not pair and segregate properly, interspecific hybridization often results in abnormalities in the meiotic process that can facilitate the process described above. Allopolyploids may not only arise more frequently than autopolyploids, but may also be more likely to become established. In addi- tion to possessing a larger genome than either of the parental species, allopoly- ploids tend to be intermediate in their characteristics, which enables them to bbe superior competitors in certain habitats. Examples: Sympatric speciation in isolated lakes. In the decades imme- diately following the new evolutionary synthesis, there was a tendency to regard allopatric speciation as the general process and sympatric speciation as the exception: a process that undoubtedly occurs in some plants and pos- sibly in a few other kinds of organisms, such as phytophagous insects and parasites, but is relatively rare. This assumption was largely due to the enor- ‘mous influence and powerful arguments of Ernst Mayr (e.g., 1942, 1963), who argued for the near universality of allopatric speciation. Recently, how- cever, the pendulum has begun to swing back as increasing evidence for sym- patric speciation has accumulated. For example, as many as 70 to 80% of angiosperm plant species are now thought to be of polyploid origin (Briggs and Walters 1984). Some of the most convincing cases of sympatric speciation involve the divergence and adaptive radiation of fishes in isolated lakes (Echelle and Kornfield 1984), There are many examples: cichlids in the Great Lakes of cen- ‘ral Africa and in the giant Quatro Cienegas spring in northern Mexico; white- fishes in the Great Lakes of eastern North America; sculpins in Lake Baikal in Siberia; herrings in Scandinavian lakes; pupfishes in Lago Chichancanab in ‘Yucatan; sticklebacks in lakes in British Columbia, These cases differ in whenthe isolation occurred and how much differentiation has taken place. At one extreme are the cichlids in Lakes Victoria, Malawi, and Tanganyika of the African Rift Valley. These fishes have been isolated in lange lakes for tens of thousands to millions of years, and a few founding lineages of cichlids have branched to produce species flocks of hundreds of species (e.g, Fryer and Iles 1972; Greenwood 1974, 1984; Kaufman and Ochumba 1993). The resulting, species exhibit enormous variation in morphology, much of it related to spe- , mee BN roars NS terpenes LOIS Soe mee C Rapes se Be Pseudotrophens Lethrinops Corematodus fuscus @ brevis shiranus Cc Rock scraper ( i Sand-digging aes ‘Scale ° insect eater m ‘eater Gi PEK eee Figure 8.10 Examples ofthe variety of head shapes, mouthparts, and feed- ing habits resulting from the adaptive radiation of cichlid ishes in Lake Malawi in eastern Africa, Thisamazing variation reflects specialization in diet due to natural seletion to reduce com- petition and exploit ecological oppor- tunities. (After Fryer and Iles 1973.) At the opposite extreme are the pupfishes of Lago Chichancanab and the sticklebacks of British Columbia, which have been isolated in small lakes for only a few thousand years as a result of changing sea and lake levels since the Pleistocene (see Chapter 7). Lago Chichancanab contains five species of Cyprin- ‘don, which have distinctive morphologies related to diet and also exhibit some degree of genetic and behavioral reproductive isolation (Figure 8.11) (Humphries and Miller 1981; Humphries 1984; Strecker et al. 1996). Small lakes in coastal British Columbia typically contain two forms of sticklebacks, benthic and pelagic, which exhibit morphological adaptations for swimming and feed- ing along the bottom or in open water, respectively (McPhail 1994). While these pupfishes and sticklebacks have diverged much less than the African cichlids, they nevertheless provide an excellent opportunity to study the roles of ecolog- ical and evolutionary processes in speciation and adaptation. While some systematists cling to hypotheses of allopatric speciation, which typically involve changing lake levels and repeated episodes of colonizationSpeciation and Extinction 243 Figure 8.11 Morphology of five forms of pupfishes (Cyprinodon) in Lago Chichancanab on the Yucatén Peninsula of Mexico. These forms have diverged sym- patrically within the last few thousand years since the Isolation ofthe saline lake from the sea. Genetic and be- hravioral studies suggest thatthe speciation process is, ‘not complete, and that some of these forms still inter- breed to some extent. The differences in size and shape and isolation, to explain speciation among these fishes, the simplest explana- tion is that differentiation bas occurred sympattically within each of these lakes. The ultimate mechanism often appears to be disruptive selection to exploit different food resources. This hypothesis is supported by the common theme of morphological and dietary divergence found among these fishes, ceven in the cases of the pupfishes and sticklebacks, in which reproductive iso- lation between some forms is only partial and hybrids are not infrequent. ‘These cases, as well as the speciation of several kinds of animals and plants within individual islands of the Hawaiian archipelago (see Chapter 12), sug- gest that sympatric speciation may be much more common than most evolu- tionary biologists have suspected. They also suggest that disruptive selection to exploit different ecological niches may often be a sufficiently powerful force to produce speciation, even in the absence of geographic isolation. Phyletic Speciation In the processes of speciation that we have described, a single lineage splits to produce two or more species. There are also cases in which one ancestral species is transformed into a single descendent species by evolutionary changes over time. This process, called phyletic speciation, is often inferred from the fossil record. Similar organisms replace one another in successively younger deposits, often without any evidence of splitting of lineages (Figure 8.12). Each major stage in such an evolutionary sequence is called a chronospecies, and is given a Latin binomial for descriptive purposes. Many examples have been cited in the literature, but relatively few have been stud- ied carefully enough that wecan be confident that the chronospecies represent an unbroken series—and not, in fact, products of speciation events that were followed by rapid extinction of all but one lineage. reflect dietary differences, and suggest that strong selec- tion for trophic differentiation is driving the sympatric speciation, (After U. Strecker)244 Chapter 8 Figure 8.12 Reconstructed evolu- tionary history ofthe Plesiapicae, a primitive primate group from North “America, based on changes in tooth size. The dashed lines indicate the in- ferred range of variation as the lin- eages evolved. The graph shows just two branching events, but many name changes. The latter illustrate “phyletic speciation” events—suffiiently large changes in a single lineage over time to ‘warrant recognition a8 nev spaces, (From Gingerich 1976a,) Figure 8.13 Ranges of dif- ferent chromosomal forms of the grasshopper Vanderrenlla insouthern Australia. These grasshoppers are extremely Similar in morphology and ecology, but ther different chromosomal arrangements effectively prevent hybridiza- tion. Their contiguously al- lopatrc, or parapatric (Le, touching but not overlap- ping), distabutions are typi- Cal of those of sibling species formed as a result of chromo- somal changes. (After White 1978) Presindapis dbus, om 5 Hes. cookei 3 Pies. fodinatus Smeets. simon BL mt ing: ti Wp i LN, gozini eee Pls. anceps N.inermetixe oP procera = Proiiodecesept She mates I 05 06 07 08 09 10 11 12 13 14 15 16 17 Log (length - width) of frst molar tooth Diversification Ecological Differentiation ‘Once new species have formed, what happens to them? Immediately after a speciation event, the resulting species are often quite similar to each other. ‘Above, we pointed out that they are most likely to diverge if they are subjected to different environments with different selective regimes. Ecological differen-tiation increases the likelihood that the species will be able to occupy overlap- ping geographic ranges. Thus it facilitates the buildup within a region of a biota of closely related, sympatric species. Gause (1934) showed in laboratory experiments with protozoars of the genus Paramecium that two species with identical resource requirements could not persist in the same environment one species was eventually outcompeted and went extinct. Ecologists have generalized this phenomenon and termed it the principle of competitive exclusion (see Hardin 1960; Miller 1967; Hutchinson 1978). A biogeographic corollary of the principle of competitive exclusion is that species that are extremely similar in their niches tend to have nonoverlapping. ‘geographic distributions, whereas species that coexist in the same area and habitat tend to differ substantially in their resource use. Perhaps the most striking example of this phenomenon is provided by so-called sibling or eryp- tic species: species that are genetically distinct, but extremely similar in their morphology and ecology. Examples include species that have recently formed through chromosomal changes. Sibling species often exhibit almost perfectly abutting, but nonoverlapping (ie., parapatric), geographic ranges, as demon- strated by numerous examples in both plants and animals (Figure 8.13). Even related species that have apparently originated by allopattic speciation and are xno longer extremely similar may competitively exclude each other from local habitats or extensive geographic areas. Examples include the kangaroo rats and chipmunks mentioned in Chapter 4 (see Figures 4.25 and 4.26). Several species of pocket gophers—fossorial rodents of the genera Thomomys and ‘Geomys—have ranges in western North America that come into contact, but do not overlap. Even though the burrows of parapatric species may be only a few ‘meters apart, the species remain separate (Figure 8.14). There is good evidence that this pattern is maintained by competitive exclusion (eg., Miller 1964; ‘Vauughan and Hansen 1964; Yaughan 1967). Conversely, numerous field studies show that when closely related species do coexist in nature, they often differ substantially in their use of limiting resources (e.g,, MacArthur 1958, 1972; Cody and Diamond 1975). Often these © Totalpoiies © T. bottae Speciation and Extinction 245 Figure 8.14 The small-scale distribution of two species of pocket gophers, as indicated by the locations of burrows of individual animals. The map encompasses approximately 1 km of & valley inthe Rocky Mountains of Colorado, Note that these morphologically and ecologically similar species come nto extremely close proximity but do not overlap. (From Vaughan 1967)246 Chapter 8 niche differences are reflected in pronounced morphological, physiological, or behavioral differences. The Galdpagos finches provide excellent examples of this phenomenon. As the finches have reinvaded inhabited islands after spe- ciating, they have diverged morphologically, behaviorally, and ecologically from other sympatric species. This process, called character displacement (Brown and Wilson 1956), has resulted in species being more different where they coexist than where they live allopatrically (see Figure 8.2). In these finches, character displacement is most apparent in the size of the beak, which enables coexisting forms to specialize on different kinds of foods (Lack 1947; Abbott et al. 1977; Schluter and Grant 1984; Schluter et al. 1985; Grant 1986; Grant and Grant 1989). Some intermediate phenotypes do occur, but strong selection against interspecific hybrids and other deviant phenotypes during pperiods of food shortage maintains the clumpy-gappy distribution of distine- tive sympatric species (see Figure 6.2). Adaptive Radiation “Adaptive radiation is the diversification of species to fill a wide variety of eco- logical niches. It occurs when a single ancestral species gives rise, through repeated episodes of speciation, to numerous kinds of descendants that become or remain sympatric. These coexisting species tend to diverge in their use of ecological resources in order to reduce interspecific competition. Such character displacement in response to competition obviously cannot occur if closely related species remain divided by physical barriers (ie, vicariant), but some differentiation will still tend to occur as the allopatric species adapt to different environments. Today, looking at the variety of living things, we can find numerous exam ples of successful lineages that have radiated to produce diversity at many lev- ls, We can, for example, consider the adaptive radiation of Hawaiian honey- creepers (Drepanidinae), a group of small perching birds that probably colonized the archipelago within the last few million years (Amadon 1950; Raikow 1976; Tarr and Fleischer 1995). Or we can examine the major radiation of placental mammals, which occurred during the early Cenozoic era, after the ‘mass extinction event that eliminated most of the giant reptiles, and procluced many of the existing mammalian orders (¢g,, Lillegraven 1972) In all such éases, the basic ecological and evolutionary processes are similar. New ecolog- ical opportunities are created by either an adaptive innovation or an environ- mental change, such as colonization of a new area or the extinction of compet ing species. These opportunities are exploited as an ancestral form repeatedly speciates, diversifies, and specializes to fill numerous ecological niches, ‘One of the most dramatic examples of adaptive radiation, mentioned above, is provided by the cichlid fishes of the lakes of Fast Africa, and is described in a fascinating book by Fryer and Iles (1972; see also Greenwood 1974, 1984; Meyer etal. 1990; Kaufman and Ochumba 1993; Johnson etal. 1996). The cich- lids have diversified morphologically and have specialized behaviorally and ecologically to fill many different niches (see Figures 8.9 and 8.10). There are herbivores and carnivores; species with mouths and teeth adapted for catch- ing tiny zooplankton, crushing snails, and eating other fishes whole; even forms specialized to feed just on the fins, scales, or eyeballs of other fishes. Islands and archipelagoes provide many other examples of adaptive radia- tion. Madagascar, with its long history of isolation from Africa and the other southern continents (see Chapter 6), has been the site of several spectacular radiations. These include not only the well-publicized lemurs (Primates), but the less well known tenrecs (a morphologically, behaviorally, and ecologically diverse endemic family, Tenrecidae, in the mammalian order Insectivora:Speciation and Extinction 247 Eisenberg and Gould 1970) and vanga shrikes (a similarly diverse group of perching birds belonging to the endemic family Vangidae). Among the many ‘examples in the Hawaiian Islands (see also Chapters 12 and 14; Wagner and Funk 1995) are Hawaiian honeycreepers of the endemic subfamily Drepanid- nae. There were about 33 species of these birds when Europeans fist visited Hawaii, although at least 10 have since gone extinct and most of the others are endangered. They are descended from a single common ancestor, now thought to be a cardueline finch that colonized from North America, probably less than 5 million years ago (Tarr and Fleischer 1995). The lineage radiated to produce an amazing variety of species, which differ conspicuously in the sizes and shapes of their beaks (Figure 8.15) and to a lesser extent in color pattern. ‘As in Darwin's finches and the African lake cichlids, ecological differentiation to exploit different niches, especially alternative food sources, seems to have been the primary process that led to the radiation of the honeycreepers. a sanguin xe oN a << Loxops sagittis Loxops viens sleinegeri aa Hemignaths ah Pseudonestor (| ES + Henignatus wilson? attrstra iS baw “emignethus Figure 8.15 The variety of beak shapes resulting from obscurus the adaptive radiation of Hawaiian honeycreepers (Drepanidinae). Compare this group with the examples Paitrostra of Galapagos finches (Figure 8.8) and African cichlid palmers fishes (Figures 89 and 8.10), (From Primack 1998.)248 Chapter 8 Figure 8.16 Adaptive radiation ‘on the phlox family, Plemoni- aceae, showing diversity of flower form reflecting different modes of pollination. A generalized beepol- linated ancestor is believed to have given rise tothe other forms, ‘most coevolved for mutualistic re- Jationships with particular kinds of animals, but some specialized for soltpollination. Plants in ether families that have specialized to use the same kinds of pollinators often have convergently evolved similar flower sizes, shapes, col- ots, odors, and nectar and/or pollen rewards (From Ehrlich and Hoi 1963) While many examples come from isolated habitats, such as islands and lakes, comparable adaptive radiations have occurred in other groups in the ‘oceans and on continents. They have also taken place on many different tem- poral and spatial scales. An ancient radiation occurred in the marine realm in the cryptically colored marine anglerfishes (Lophiiformes), producing the shallow-water frogfishes (Antenniamt), the open-ocean sargassum fish (Histrio histrio), the stingraylike batfishes (Ogcocephalidae), and a variety of deep- ‘water bioluminescent forms (suborder Ceratoidea). In plants, a group that has radiated over the past 20 million years on the North American continent is the phlox family (Polemoniaceae). Within this single family, flower form and color hhave become amazingly variable as different species have adapted to be polli- nated by hawkmoths, bees, butterflies, flies, or hummingbirds, and some have ‘become specialized for self-pollination (Figure 8.16). Australia, the most iso- lated continent, is the site of many spectacular radiations: marsupial mam- mals, lizards of the genera Clenotus and Varanus, and plants of the genera Eucalyptus, Melaleuca, and Acacia. ‘Whereas many genera and families exhibit a fascinating variety of ways of life, many others are extremely monotonous, differing mainly in minute struc- tural details. Taxa that have changed only slightly over evolutionary time apparently are good at what they do and have not had the genetic flexibility or ecological opportunity to shift adaptive strategies. The wide variation in rates and degrees of divergence makes it difficult to generalize about the diversifi- cation of higher taxa and the influence of geography on adaptive radiation. The many examples of spectacular adaptive radiations on islands (including ‘Madagascar and Australia) seem to show the importance of long historical iso- lation in these cases. Equally impressive radiations in less isolated settings, however, such as those of desert rodents of the family Heteromyidae in south- ‘western North America, the darters of the fish genus Etheostoma in the Missis- Self pollinating Gia inconspicue Hawks Ipomopss - iro B estes Ee samdens Ces fenton ieries Eston Homminghirds ecjemim Ipomoea Pee mo & Long Clestogamous, seltpollinating Gila Spendens grant _ Polemonitom meranthon Polemonturncaerleurssippi River drainage, and the spiny, succulent plants of the family Cactaceae in the arid regions of North and South America, suggest that long and nearly complete geographic isolation is not necessary. Comparative studies that are attempting to assess the influence of phylogenetic relationships and evolu tionary constraints (see Chapter 11; Felsenstein 1985; Brooks and McLennan 1991; Harvey and Pagel 1991) promise to contribute importantly to our under- standing of the enormous differences in rates of speciation and adaptive dif- ferentiation among lineages, Extinction Ecological Processes Although all living organisms represent a continuous evolutionary lineage extending billions of years back to the origin of life, the ultimate fate of every species is extinction. This can be appreciated by taking a brief glance at the fo: sil record. The earth was teeming with life 100 million years ago. Both terres- trial and aquatic habitats were occupied by diverse biotas that formed com- plex ecological communities, However, the species and genera—and many of the families and orders—that were dominant then have been eliminated or drastically reduced by extinction, and have been replaced by new lineages. On land, dinosaurs and other reptilian groups have been replaced by birds and mammals, while ferns and gymnosperms have been largely supplanted by angiosperms. In the oceans, cephalopod mollusks have been supplanted by teleost fishes, while icthyoseurs and mesosaurs (reptiles) have been replaced by dolphins, whales, seals, and sea lions (mammals). Extinctions have appar- cently occurred continuously throughout the history of life, although the fossil record also catalogues occasional episodes of widespread disaster when much of the earth’s biota was wiped out, apparently by rapid and drastic environ- mental change (Raup and Sepkoski 1982). Not surprisingly, extinctions have hhad a major influence not only on the kinds of organisms in existence at any given time, but also on the geographic distributions of those now extinet forms and the contemporary lineages that are descended from them. Several authors have likened the evolutionary history of life to a continual race with no winners, only losers—those species that become extinct. This view is probably best expressed in Van Valen’s (1973b) Red Queen hypothe- sis, named for the Red Queen in Lewis Carroll’s Through the Looking Glass, who said “It takes all the running you can do to keep in the same place.” The idea is that a species must continually evolve in order to keep pace with an environment that is perpetually changing, not just because abiotic conditions are shifting, but also because all the other species are evolving, altering the availability of resources and the patterns and processes of biotic interactions. ‘Those species that cannot keep up with the changes become extinct, but others do well temporarily and speciate to produce new forms. Van Valen points out thet the probability of a species becoming extinct appears to be independent of its evolutionary age, but not of its taxonomic and ecological status. Certain taxonomic and ecological groups have consis- tently higher rates of extinction than others. For example, apparently due to their lower extinction rates, small and herbivorous mammals are found on more and smaller islands than large or carnivorous species (Brown 1971b; Heaney 1986; Lawlor 1986). This appears to be a general pattern (see Van Valen 1973a). Somewhat similarly, differences in diversity and duration in the fossil record among lineages of marine invertebrates are correlated with char- acteristics of their life history, as we shall see below. Speciation and Extinction 249250. Chapter 8 Figure 8.17 Output of a mathemati- cal model showing how estimated time to extinction depends on two de- ‘mographic characteristics of a popula- tion: equilibrial population density, oF carrying capacity, (K) and the atio of birth rate (8 to death rate () The ‘graphs show that the probability of ex- tinction is high (expected time to ex: tinction is low) when populations are small and birth rates are low relative to death rates, but decreases rapidly as these demographic parameters in- crease. (From MacArthur and iNilson 1967) ‘Some researchers have developed mathematical models to predict a popu- lation’s vulnerability to extinction based on its demographic characteristics (MacArthur and Wilson 1967; Richter-Dyn and Goel 1972; Leigh 1981; Gilpin and Hanski 1991). All populations experience fluctuations in size as a result of variations in environmental conditions and the activities of their enemies, When populations become very small, however, purely chance factors, such as random variations in the sex ratio, can also affect their abundance. The math- ematical models show that, in general, the smaller a population becomes, the lower its ratio of births to deaths (see Equation 4.1), and the longer it remains at low numbers, the more vulnerable it is to extinction. A population with a low birth rate, especially when coupled with a high death rate, cannot recover rapidly from a temporary reduction in numbers. The long-term overall popu- lation size is probably the most important factor. The models suggest that probability of extinction increases nonlinearly as population size decreases, and becomes very high when population size becomes and remains very low—say, fewer than 100 individuals (Figure 8.17). These mathematical mod- ls are based on the intrinsic demographic characteristics of populations, but it is important to recognize that changes in extrinsic environmental conditions are likely to be the cause of the changes in those characteristics that ultimately lead to extinction. Information on how intrinsic demographic and extrinsic ecological factors interact to cause extinction is difficult to obtain and interpret because extine- tions of species, with the exception of those caused by humans, are rarely observed. Researchers have gained valuable insights, however, by studying the cffects of these factors on the tumover of small, isolated subpopulations within ametapopulation (Gilpin and Hanski 1991; see also Chapters 4 and 14). One particularly well-documented example is provided by the work of Smith (1974, 1980) on pikas (Ochotona princeps). Pikas are small relatives of rabbits that live in rock slides and boulder fields in the mountainous regions of west- em North America. Smith carefully monitored pikas in the Sierra Nevada of California that had colonized the rock piles left by a mining operation. These ‘mine tailings functioned as habitat islands for the pikas in a sea of sagebrush habitat. Smith was able to document extinctions of subpopulations by census- I | zo 100) 10 Time to extinction (years) bya 1.01 wa=05 — bet I 101001000 10100-1000 Equilbral population size (K)Speciation and Extinction 251 Table 8.2 Estimated time to extinction for pika subpopulations Population Birth rate Death rate Time to extinction (eumber of individuals) (per capita per year) (per capita per year) (years) K 6 a F 1 035 0.00 29 2 038 163 69 3 035 2a 462 4 035 284 4051 5 035 315 37515 Source: Data from Smith 1974, 1986 Note: The populations represented here occupy habitat islands of varying size (se Figure 8.17) Per capita birth and death rates were determined from the age structure ofthis population. A mathematical model, based on the model of MacArthur and Wilson (1967), predicts that only ‘very small populations (K <3 individuals) should have measurable ates of extinction oving $2 ‘ordinary random demographic scustions, This prediction was confirmed by Smiths subse- {quent measurement of population furnover on these same islands during a 5-year period. ing the rock piles initially in 1972 and then again in 1977. The repeat censuses documented both extinctions of previously existing subpopulations and colo- nizations of previously uninhabited rock piles. From data on the birth and death rates of pikas and the sizes and degree of isolation of the rock piles, Smith and colleagues developed a stochastic model that quite accurately pre- dicted the frequency of extinction and colonization events as a function of these factors (Hanski and Smith, pers. comm.) (Table 8.2). Somewhat similarly, Lomolino (1984, 1993) and Crowell (1986) documented the extinction and immigration of small mammals on islands in the St. Lawrence River, Lake Huron, and the Gulf of Maine. Even though these studies are concerned with the turnover of small, isolated subpopulations rather than extinctions of entire species, they illustrate how both intrinsic demographic characteristics and. extrinsic environmental conditions influence the extinction process. Recent Extinctions Over the last 200 years, humans have caused the extinctions of thousands of species. We are undoubtedly unaware of many species of microbes and small animals and plants that have disappeared, but the demise of some larger, more spectacular organisms is well documented. The recent reductions in popula- tions, contractions of geographic ranges, and extinctions of species caused by humans will be considered in more detail in Chapter 18. We will present a few examples here, however, to illustrate some of the processes involved in extinc- tions, because we have much more information about some of these recent extinctions than about most of those evidenced in the fossil record. ‘The passenger pigeon (Ectopistes migratorius) was incredibly abundant in eastern North America when the first European colonists arrived. Estimates of the total population size are in the millions, perhaps billions. Because the pigeons traveled in dense flocks numbering in the thousands, feeding on beechnuts, acorns, and other abundant seeds and fruits, and nested in huge aggregations, they were very vulnerable to humans, who hunted them for food. In the 1870s, 2000 to 3000 birds were often taken in one net in a single day, and 100 barrels of pigeons per day were shipped to New York City for weeks on end, By 1890 the birds had virtually disappeared. In 1914 the last known passenger pigeon died in the Cincinnati Zoo (Pearson 1936). Similar252 Chapter 8 stories could be told about the demise of the great auk, Carolina parakeet, and. Steller’s sea cow. Only a combination of luck and belated conservation action hhas prevented the whooping crane, trumpeter swan, bison, sea otter, gray whale, and northem elephant seal from suffering similar fates. ‘A different lesson can be drawn from the demise of the American chestnut ‘tree (Cistaren dentata). Along with beech, maple, oak, and hickory, the chestnut ‘was one of the most abundant trees in the deciduous forests of eastern North America. In 1904 a pathogenic fungus (Endathia parasitica) was accidentally introduced, apparently from Asia, where it attacks a related but less suscepti- ble species of chestnut. The disease spread rapidly (Metcalfe and Collins 1911), and within 40 years, mature chestnuts were virtually eliminated from their entire range. In some areas, scattered small trees that have sprouted from sur- viving root stock can still be found. Unfortunately, these are usually attacked by the disease and killed before they can reach reproductive size, soit is ques- tionable whether the chestnut can much longer avoid absolute extinction. Sim- ilar cases of biological warfare due to introduced pathogens are the near extinction of the American elm due to Dutch elm disease, of native Hawaiian birds due to avian malaria (see Chapter 4), and of native peoples on oceanic islands, and perhaps even on the American continents, due to smallpox, ‘measles, diphtheria, and other diseases brought by European invaders, One of the best-documented cases of local extinction of multiple species is the loss of bird species from Barro Colorado Island in Panama (see Figure 9.16). Prior to the early 1900s the island did not exist; it was simply a hill in a tract of tropical lowland forest. During the construction of the Panama Canal, the Chagres River was dammed, and the rising waters of Gatun Lake covered the adjacent lowland areas, creating Barro Colorado, an island of about 16 km’. Despite its relatively large size, Barro Colorado no longer contains many of its original bird species. Because the Smithsonian Institution has long operated a biological research station on the island, its biota is well known, and some of the extinctions are well documented. Using these records, Willis (1974) caleu- lated conservatively that atleast 17 species had been lost from a total land bird fauna in excess of 150 species. More recently, by comparing the avifauna of the {sland with that of a mainland site of similar size and habitat, Karr (1982) con- cluded that at least 50 species have become extinct on the island since its iso- lation. Although habitat changes may have contributed to the demise of some forms, most of the missing species normally occur at low densities, and it appears that when the small populations present on the island died out, they were not replaced by colonists from across the narrow water gap. ‘The above examples illustrate the vulnerability of many species to environ- ‘mental changes caused by modern humans (see also Chapters 17 and 18). Humans do not need to have guns, agriculture, or European culture to cause extinctions, however. Aboriginal humans almost certainly played a major role in many extinctions documented in the fossil record, as we saw in Chapter 7. (On the other hand, the capacity of some species to recover from low numbers is amazing, Two species of marine mammals that inhabit the Pacific coast of North America, the northem elephant seal (Mirouga angustirostris) and the sea otter (Enhydra lutris), were hunted almost to extinction for their fat and fur, respectively. Tiny populations managed to escape detection, however, and once protected, increased rapidly to produce large, healthy populations Another Pacific marine mammal, the gray whale (Eschrichtius robustus), has been increasing reassuringly following the protection of its breeding grounds off Baja California and the cessation of hunting (Rice and Wolman 1971), and ‘was recently removed from the U.S. Endangered Species List. Several bird species that were hunted to near extinction in the late 1800s for feathers tosupply the millinery industry, including trumpeter swans, sandhill cranes, and great and snowy egrets, are again abundant. Extinctions in the Fossil Record The fossil record provides abundant evidence of extinctions, but often provides only tantalizing clues to theit causes, In many cases the fossil record is complete enough to show that many diverse species became extinct virtually simultane- ously over relatively short periods of geological time. We can infer that such mass extinctions were caused by some drastic, widespread environmental change, but the exact nature of the perturbation and its effect on the organisms concemed is often difficult to deduce clearly. Long-standing, vigorous debates about the causes of mass extinctions mark the paleontological literature. ‘One of the most recent episodes of mass extinction was the disappearance of the Pleistocene megafauna of North and South America between 15,000 and '8000 years ago. The cause of this dramatic event is still the subject of contro- versy, as we saw in Chapter 7. Originally, paleontologists favored hypoth invoking climatic change. The idea that aboriginal humans played a major role, advanced by Paul Martin in the 1960s and known as the “overkill hypothesis,” was initially rejected by most paleontologists. Multiple lines of accumulating evidence, however, have shifted the balance, causing many sci- entists to conclude that humans almost certainly played a significant, and per- haps a pivotal, role in the extinctions of the megafauna (e.g,, Martin and Klein 1984; Owen-Smith 1987, 1989). Examples of additional extinctions caused or threatened by moder humans will be discussed in detail in Chapter 17. ‘The causes of other mass extinctions that occurred even longer ago have also been highly controversial. The two most dramatic episodes saw the dis- appearance of the dinosaurs and many other groups of terrestrial and marine organisms at the end of the Cretaceous period, about 65 million years ago, and of even more species and higher taxa, particularly marine organisms, at the boundary between the Permian and the Triassic periods, about 225 million years ago (see Raup 1979; Raup and Sepkoski 1982). Raup estimated that 88 to 36% of all marine species then in existence went extinct at the end of the Per- mian. The causes most often invoked for these and other mass extinctions are large, rapid changes in the climate of the earth: either global cooling, with resulting continental glaciation and exposure of continental shelves, or global warming, with associated rising sea levels and inundation of continental shelves (eg., Stanley 1984). But other explanations, including continental drift (eg, Schopf 1974) and reorganization of interaction in ecological communities (Bak 1996) have had their proponents. While the causes of the Permo-Triassic event remain poorly understood, there is now little doubt about the cause of the Cretaceous-Tertiary event. Its, discovery is one of the most exciting detective stories in the recent earth sci- ‘ences, rivaling the development of plate tectonic theory. It has long been apparent that the end of the Cretaceous was a time of major change. The Cre- taceous-Tertiary (K-T) boundary was defined based on dramatic changes in the fossil record. Not only did major groups of previously dominant organ- isms (such as dinosaurs on land and ammonites in the oceans) go extinct, but there were also major changes in the abundance and species diversity of the lineages that survived (e.g,, dramatic increases in birds and mammals on land and teleost fishes in the oceans; decreases in marine cephalopod mollusks). Until the early 1980s these changes were generally thought to have occurred over several million years and to have been caused by climatic change. In 1980 three scientists at the University of California at Berkeley (Alvarez et al. 1980, 1984) suggested a radically new hypothesis: an asteroid impact, Ini- Speciation and Extinction 253254 Chapter 8 tially, this sounded like an idea from a science fiction movie and was ridiculed by many established earth scientists. Nevertheless, the group led by Walter Alvarez presented intriguing data and a testable hypothesis. The asteroid impact hypothesis was based on the occurrence in rock strata that spanned the K-T boundary of a layer highly enriched in the element iridium (Ir). Iridium is zare in the earth's crust, but is often present in high concentrations in materi- als of extraterrestrial origin (meteorites and asteroids). The Alvarez group hypothesized that the iridium-enriched layer was produced by the dust injected into the atmosphere and circulated around the earth following the impact of a large asteroid. The dust presumably blocked solar radiation and. resulted in rapid global cooling, which in turn caused the extinction of the dinosaurs and other lineages. ‘A strength of the Alvarez. hypothesis was that it made testable predictions (Alvarez et al. 1984). First, it predicted that when an iridium-enriched layer occurred near the K-T boundary, it would always separate Cretaceous rocks below from Tertiary strata above. This prediction led to efforts to find strati- graphic sequences spanning the K-T boundary, to search for an iridium- enriched stratum, and to date the underlying and overlying rocks. Many inde- pendent studies of localities throughout the world confirmed the prediction: when present, the iridium-enriched layer marked the K-T boundary. Second, the hypothesis predicted that the vast majority of extinctions should have ‘occurred right at the K-T boundary. Previous interpretations of fossil remains had suggested that some taxa disappeared millions of years before or after the K-T boundary. More accurate dating of fossil remains, however—especially with reference to the telltale iridium-enriched layer, when present—increas- ingly supported the hypothesis: the extinctions were concentrated during a very brief period. Third, an asteroid impact and resulting global cooling would be expected to lead to differential extinction or survival of different kinds of organisms depending on their life histories and ecologies. And indeed, the K- T extinctions were highly selective. Those groups, with capacities for body temperature regulation, such as endothermic birds and mammals, and those with life history stages that would be resistant to a brief but intense cold stress, such as seed plants, insects, and freshwater invertebrates, suffered fewer extinctions than many other kinds of organisms. Finally, the hypothesis predicted that the crater formed by the asteroid impact might actually be discovered, and suggested that the thickness of the iridium-enriched stratum should provide clues to its location. Obtaining evi- dence bearing directly on this prediction initially seemed to be a long shot. No Janown meteorite craters had the appropriate combination of size and age to be good candidates. Further, since most of the earth’s surface is ocean and most Of the seafloor is young, there was a high probability that the impact occurred in the ocean and that the crater had long since been subducted into an ocean trench (see Chapter 6). However, mapping of the increasing data on the irid- jum-enriched stratum showed a clear geographic pattern, with the thickest layers in the Caribbean region. Then came the definitive find: the discovery of a crater—of the right size and age—on the continental shelf off the coast of ‘Yucatén (Swisher et al. 1992). ‘So we now know that an asteroid did strike the earth about 65 million years ago. It appears to have caused the extinction of the dinosaurs, ammonites, and many other organisms, and in so doing, to have opened the way for mam- mals, teleost fishes, and other lineages to rise to their present dominance. While the major features of this event are now well documented, many pieces of the story are not. How much was the earth cooled, and how long did the cold period last? Beyond the differences in life history and ecology mentionedabove, what determined which species and clades died out and which sur- vived? Clearly, even such an unprecedented and unpredictable event as the impact of an extraterrestrial body did not cause “random extinctions. Instead, it acted as a severe filter, eliminating many lineages, allowing others to pass through, and causing revolutionary changes in the composition of the earth’s biota that have endured for 65 million years. Species Selection Processes of Species Selection ‘The historical pattern of speciation and extinction has had a major influence on the taxonomic diversity and geographic distribution of living things Episodic events such as explosive adaptive radiations and mass extinctions have been particularly important. The aftermath of the K-T extinction event ‘makes a point that is also illustrated by other parts of the fossil record: lineages, of organisms have not been equally successful, and even the most successful lineages have been dominant during different periods of earth history and have prospered for different lengths of time. Some lineages have radiated rapidly to leave many descendants; others have survived virtually unchanged for millions of years; still others have disappeared quickly, leaving no descen- dants. Paleontologists and biologists have long recognized that certain lin- eages appear to possess particular traits that result in high speciation rates or low extinction rates, thereby leading to adaptive radiation and relative evolu- tionary success compared with those groups that die out or barely maintain ‘themselves. ‘As mentioned in the discussion of macroevolution above, the differential survival and proliferation of species over geological time has come to be termed species selection (Stanley 1979), by analogy to the differential survival and reproduction of individuals (individual selection), which has traditionally been considered the primary mechanism of evolutionary change by natural selection. Species selection and individual selection should be viewed not as totally different biological processes, but as the consequences of generally sim- ilar ecological and genetic processes operating at different levels of biological organization. The same conditions (¢.g,, rapid environmental changes) that cause large differences in the birth and death rates of individuals of different genotypes and thus result in rapid evolution by individual selection are also likely to lead to differential multiplication and survival of species and thus to result in rapid evolution by species selection. Rapid evolution by individual selection is likely to be a primary cause of high speciation rates, which con- tribute to rapid phyletic diversification by species selection. Examples of Species Selection To some extent the fate of evolutionary lineages is a matter of chance and opportunity—it depends on a species with particular traits being in a favor- able place at an opportune time. As emphasized above, many adaptive radia- tions begin when a population either colonizes a new area or evolves some new trait that substantially increases its fitness in a particular environment (Gimpson 1952a). In either case, the species is suddenly presented with new ecological opportunities, which stimulate further rapid evolution and specia- tion. The Cenozoic radiations of mammals illustrate the influence of both of the above factors. During the late Mesozoic the ancestors of modern placental mammals acquired several new traits, including higher metabolic rates, improved temperature regulation, and new mechanisms of nourishing theit Speciation and Extinction 255256 Chapter 8 ure 8.18 The “explo- sive” radiation of placental ‘mammals during the Ceno- zoic, illustrated by the rapid increase in number of fami- lies. This radiation occurred after the K-T mass extinction event as mammals diverged and specialized to take ad- vantage of ecological oppor- tunities presented by the ex- tinction of the dinosaurs and other groups of previously dominant reptiles. (After Lillegraven 1972.) developing young. These traits represented major advances over their reptilian ancestors and over other kinds of primitive mammals, including monotremes, marsupials, and some now extinct groups. The extinction of the dinosaurs and other vertebrate groups at the end of the Cretaceous eliminated their rivals and provided them with new ecological opportunities. Immediately after- ward, in the early Cenozoic, a relatively few lineages of placental mammals radiated explosively (Figure 8.18). They not only “replaced” the extinct reptil- ian groups, but also diversified at the expense of other mammalian lineages, such as the “primitive” docodonts and the rodentlike multituberculates, that had survived the K-T mass extinction. ‘The radiation of placental mammals occurred throughout the world except in Australia and, for most of its Cenozoic history, South America. On these iso- lated continents, surrounded by ocean barriers, egg-laying monotremes, pouched marsupials, and other kinds of primitive mammals persisted. In the absence of the dominant reptiles, some of them underwent their own radia- tions. South America subsequently was colonized by many groups of placen- tal mammals from North America, and many of the original South American taxa became extinct (see Chapter 16). Australia has remained isolated right up to the present. Two groups of egg-laying monotremes (duck-billed platypus and echidna) survived, and the marsupials underwent an extensive radiation, giving rise to many families and diverse morphological and ecological types. These include a sand-burrowing “mole” (Notorydtidae), small to medium- sized insectivores and carnivores, some called marsupial “mice,” “cats,” and “wolves” (Dasyuridae), numbats (Myrmecobiidae), possums, gliders, and koalas (Phalangeridae), bandicoots (Peramelidae), wombats (Phascolomiidae), and a wide variety of wallabies and kangaroos (Macropodidae). Prior to the 129) nio| 100] Ss Mammalian families Number upper | Paleocene Bocene Oiigoctne | oct It 3 Chacous g a r Milion 65 «055 50 45-40-9525, SOS years ar,Pleistocene and the arrival of humans, dogs (dingoes), and other mammals, that the humans imported, only two orders of placental land mammals, rodents and bats, managed to colonize Australia from Asia across water bar- riers. The rodents diversified dramatically, after at least two different coloniza- tion events, to produce about 80 species, most belonging to endemic gentera. ‘These include water rats (Hydromys), desert hopping mice (Notomys), and stick nest builders (Leporillus), which are ecologically and morphologically similar to North American muskrats (Neofiber), kangaroo rats (Dipodomys), and pack- rats (Neoloma), respectively (Keast 1970, 1972c). {In the absence of a historical event that eliminated competitors or provided access to a new area, radiations often were slower, and the buildup of diver- sity took longer. Many such radiations apparently occurred when some evol- tionary innovation gave an ancestral species an advantage over coexisting organisms. Despite its apparent superiority, however, it usually took consider able time for the founding lineage to speciate, diversify ecologically, and sup- plant other groups of organisms that were already present. An example is pro- vided by the neogastropods, a group of specialized, predatory marine snails that originated in the Cretaceous, 130 million years ago, and has gradually diversified to become a dominant invertebrate group. Another is provided by the angiosperm plants, which also originated in the Cretaceous. They pos- sessed a number of structural and functional innovations in reproductive biol- ogy that, among other things, allowed them to evolve mutualistic associations with the animals that pollinate their flowers and disperse their seeds. Despite these advantages, however, it took until the mid-Cenozoic—about 100 million years—for the angiosperms to largely supplant the previously dominant ferns and gymnosperms (Figure &.19; Niklas et al. 1983; Knoll 1986; Taylor 1996). ‘The importance of evolutionary innovations, or atleast particular combina- tions of adaptive tras, is illustrated by macroevolutionary and biogeographic patterns in mollusks. There is an interesting relationship between speciation rate, geographic distribution, and mode of larval dispersal among these groups (Jackson 1974; Hansen 1980; Jablonski and Lutz 1980; Jablonski 1982). Some groups have planktotrophic larvae—juvenile stages that drift passively in the ocean—whereas others brood their offspring or have other specializa- tions that do not involve their young being dispersed in the plankton. The mode of larval dispersal can be determined for fossil as well as for recent forms because an individual's original larval shell is preserved as part of its adult shell, which is readily fossilized. Molluscan species with planktotrophic larvae tend to have larger geographic ranges (Figure 8.20) and lower specia- tion rates than related species whose young rarely disperse far from their par- 8 Speciation and Extinction 257 2 9 B g oor Figure 8.19 ‘The relatively gradual radiation of angiosperms £ as illustrated by changing composition of fossil floras repre~ a) senting past communities. Although innovations in reprodwc- 5 tive biology apparently gave the angiosperms advantages over z the previously dominant gymnosperms, the increase in the for- 3 other plants mer and decreas inthe latter took over 100 million years. The angiosperms ultimately attained much higher diversity than a oe their gymnosperm progenitors although some gymnosperms, Millon years 32, 1986.) such as conifers and cycads, still survive today. (After Knoll,258 Chapter 8 (a) 6) Pnkoweri 1° ¥ al j fe Eo ee ens ie Ceoepnge en) Deaton ine oye) Percentage of species Nonplanktotrophic 7 «0 50 “ 30 20 20 ° 2000-3000 4000 e102 14 16 Gexgapie rng: Oo) ‘Danton ions yam) Figure 8.20 Relationship between mode of larval dispersal, extent of geographic range (A), and survival time in the fossil record (B) of late Cretaceous mollusks on the east coast of North America. Note that species whose larvae can disperse long, distances inthe plankton (planktotrophic species) tended to have larger geographic ranges and lower extinction rates (longer survival times) than those species whose Jarvae settle close to their parents (ronplanktotrophic species). (After Jablonski 1982) ents, Limited dispersal of offspring presumably reduces gene flow, enables populations to adapt to local conditions, and thus facilitates genetic differen- tiation and allopatric speciation. On the other hand, because small specialized populations are also particularly vulnerable to extinction, nonplanktotrophic species tend to persist in the fossil record for shorter periods of time than do those with planktotrophic larvae (Figure 8.208). ‘As implied by this example, patterns of species extinction, which depend in part on the characteristics ofthe organisms themselves, can influence the evo- Jutionary histories of lineages by species selection, Over a period of 600 mil- lion years, one group of marine bottom-dwelling invertebrates, the clams (Mollusca, class Bivalvia), has been replacing a phylum, the brachiopods (Bra~ chiopoda) (Figure 8.21). Because these two groups have superficially similar morphology, feeding habits, and habitat requirements, it had long been thought that the clams were supplanting the brachiopods by competitive exclusion (Elliot 1951). In fact, species of the two groups may compete signifi- cantly where they occur together, but careful examination of the fossil record indicates that the increase of clams and the dramatic decline of brachiopods ‘was also facilitated by mass extinctions that eliminated many more taxa of brachiopods than of clams (Gould and Calloway 1980). Valentine and Jablon-Speciation and Extinction 259 s00 aa + clans ‘0 “A Kt masgexintion on : Rermian mae extinction i v © an on . . 2 . : 100 7 oF aoe cot 80 Oo ogo temee ° 600 400 300 200 100 0 ge niion yeas a u Figure 8.21. ‘The “replacement”, over ski (1982) suggest that the brachiopods are differentially susceptible to cata- strophic extinction because they do not have planktotrophic larvae, but instead. brood their young or produce larvae that spend only a brief time in the plank- ton. As noted above, marine invertebrates with nonplanktotrophic larvae tend. to have restricted geographic distributions and high extinction rates. Bra- chiopods have largely been eliminated from shallow-water habitats, where they are exposed to environmental fluctuations, but some forms persist in deep waters, where their mode of reproduction is less disadvantageous. ‘The fossil record documents the origination and extinction of lineages at all taxonomic levels, from species to phyla. Many of these lineages radiated to produce considerable morphological and ecological diversity, and some spread throughout the wor'd, But success was almost invariably fleeting: most groups declined in diversity and ultimately went extinct. Sometimes their fates were due primarily to chance events, such as genetic drift, random extinctions of small populations, vicariant isolation due to plate tectonics, or the collision of an asteroid with the earth. Often, however, their biological attributes, shaped by the microevolutionary force of natural selection and the macroevolutionary force of species selection, played key roles. The more we learn about the history of life, the more we appreciate the influence of the non- random biological processes that have shaped the patterns of speciation and extinction, 4600-million-yeae period, of bra- chiopodis (phylum Brachiopoda) by clams (phylum Mollusca, class Bi- valvia) This sift in dominance has often been attributed to competition because the two groups are generally similar in morphology and ecology. While competition may have played an important role, so did several mass ex- tinction events after both the Permian and the K-T mass extinctions, bra- chiopods declined in diversity, while clams increased. (After Gould and Cal- loway 1980.)