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The semantics of evolutionary adaptation: clarification and evaluation

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The semantics of evolutionary adaptation:

clarification and evaluation

G.P. Cheplick

To cite this article: G.P. Cheplick (2020): The semantics of evolutionary adaptation: clarification
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JOURNAL OF BIOLOGICAL EDUCATION
https://doi.org/10.1080/00219266.2020.1739116

The semantics of evolutionary adaptation: clarification and

evaluation
G.P. Cheplick
Biology Program, Plant Science Subprogram, The Graduate Center, City University of New York, New York, NY, USA

ABSTRACT KEYWORDS
A complex terminology developed around the evolutionary concept of Adaptive evolution; adaptive
adaptation. One definition of adaptation is synonymous with adaptive evolu- value; natural selection;
tion and denotes a process of population change driven by natural selection resurrection studies
resulting in individuals better able to survive and reproduce in a particular
environment (compared to the population before the process began). This
places adaptation at a hypothetical end point in a temporal sequence and
can be difficult to use because the phenotypic composition of earlier, non-
adapted populations is unknown. However, resurrection experiments can
provide comparative data on populations before and after adaptation. The
process of adaptation is a corollary to the well-described precepts of natural
selection found in textbooks. Adaptation also denotes any trait that increases
an organism’s fitness relative to individuals lacking it. This ‘all or none’
concept of adaptation limits its usefulness because most traits are quantita-
tive. Leaf pubescence, a quantitative trait showing phenotypic and genetic
variation in plant species, is used to illustrate adaptive value and significance.
Historical application of adaptation has ranged from individuals to popula-
tions to species and encompassed molecular and phenotypic traits. Although
exaptation and maladaptation have some heuristic utility, ‘pre-adaptation’ is
best avoided because it does not reflect adaptive evolution.

The difficulty of the concept adaptation is best documented by the incessant efforts of authors to analyse it,
describe it, and define it (Mayr 1983, 324).

Adaptation is a term readily used by students and researchers in evolutionary biology as if its
meaning was self-evident. However, there are multiple ways the word and its derivative forms can
be used and its precise meaning cannot always be gauged by its usage (Stern 1970; Munson 1971;
Bock 1980; Reeve and Sherman 1993). Confounding the issue, the term is also used by non-
scientists to express the ability of individuals (usually people) to adjust to a new environment
with changed conditions (Latta 2010). Of course, this usage does not imply an evolutionary process
at all, although it appears superficially similar to biological adaptation.
A variety of misconceptions have been documented regarding concepts important in under-
standing biological evolution, especially natural selection and adaptation (Nehm and Reilly 2007;
Kampourakis and Zogza 2008; Gregory 2009). Young students often comprehend nature intuitively
in teleological ways (Blancke et al. 2014) and purpose-driven explanations for evolutionary adapta-
tion can persist into high school and post-secondary education (Gregory 2009). This leads to
misleading ideas of natural selection whereby organisms change in response to their environment
as a need to ‘adapt’ to specific conditions. This is similar to the non-scientific use of adaptive
terminology to depict the adjustment of organisms to changed environmental conditions.
Teleological explanations for biological processes have also been problematical to the historical

CONTACT G.P. Cheplick gregory.cheplick@csi.cuny.edu

© 2020 Royal Society of Biology
2 G. P. CHEPLICK

development of evolutionary concepts (Mayr 1982). A substantial part of the misunderstanding of

how adaptations arise during biological evolution stems from a failure to apply ‘population
thinking’ (Mayr 1982, 45) when considering processes such as adaptive evolution (Stern 1970).
Given a long-established recognition of evolutionary adaptation as a major concept in biology
(Williams 1966; Amundson 1996), a clarification and evaluation of the terms and phrases related to
adaptation should prove valuable to instructors who teach evolutionary concepts in their classes.
A complex web of terms and phrases have developed around the concept of adaptation. To
illustrate the myriad phrases that have been derived from the root word adapt, consider the
following list of terms and phrases:

Adaptedness Adaptive landscape

Adaptive peak Adaptive potential
Adaptive radiation Adaptive significance
Adaptive value Co-adaptation
Exaptation Local adaptation
Maladaptation Molecular adaptation
Pre-adaptation

This lengthy set indicates a plethora of ‘adaptive’ variations on a general theme that is difficult to
delimit and not entirely clear. Use of a common language to depict the process of adaptation at the
population level as well as the traits that result at the individual level should help instructors choose
the correct way to phrase interpretations of evolutionary phenomena while avoiding the pitfalls of
teleology and anthropomorphic misconceptions (Blancke et al. 2014; Gregory 2009).
The objectives of this article are (1) to clarify usage of terms associated with evolutionary
adaptation as a process and as a trait, (2) to provide a detailed example of how a phenotypic trait
(leaf pubescence) might be investigated to determine its adaptive value and adaptive significance,
(3) to consider how the term adaptation has been applied to different levels within the biological
hierarchy of life, and (4) to briefly explore the utility of terms closely allied to adaptation that have
been used to depict the various results of adaptive evolution. In the interest of clarification, I begin
by considering two familiar usages of the term adaptation: as a population process and as a specific
trait that results from the process (Amundson 1996).

Adaptation as a population process

One use of the term adaptation is synonymous with ‘adaptive evolution’ and denotes a process of
population change driven by natural selection that results in a group of individuals better able to survive
and reproduce in a particular environment (compared to the population before the process began).
There are some difficulties with this definition. It clearly depicts an emergent microevolutionary process
for which there is no definitive beginning or end (Cooper 2017). Adaptive evolution is a dynamic,
ongoing process that continually fine-tunes the match or fit between organisms and their environment
as selection favours some genotypes (and their phenotypes) over others (Larson 2009). Perfect adapta-
tion of a population to a habitat never arises because conditions are highly variable in space and time.
Features evolved in relation to one set of conditions might not be adaptive under a new set of conditions.
It must be recognised that, although it is individuals that possess the phenotypic characteristics that
are adaptive in a particular environment, it is the population that has undergone the evolutionary process
of adaptation. Herein lies the conflict between adaptation in popular usage versus its use by evolutionary
biologists. The popular usage of adaptation as the adjustment of individuals to changed conditions
actually denotes acclimation or phenotypic plasticity as defined by biologists (Latta 2010). An individual
genotype may respond to changed environmental conditions by adjusting its morphology and physiol-
ogy in specific ways. Although this adjustment can have adaptive value, a change at the individual level
does not represent adaptive evolution as a population process.
 JOURNAL OF BIOLOGICAL EDUCATION 3

Evolutionary adaptation can be visualised as a continuous process that depends on a variable

population gene pool repeatedly exposed to a particular set of selective agents (Figure 1). The
genetic composition of the pool may be altered by random mutation and gene flow into the
population via direct movement (animals) or by pollen and seed dispersal (plants) (Ellstrand
2014). In this way, new alleles are introduced into the gene pool. In addition, sexual reproduction
will produce novel combinations of alleles and variable phenotypes that show differences in the
ability to survive and reproduce under the prevailing environmental conditions (Bell 2008). The
episodes of selection in Figure 1 are due to the effects of abiotic and biotic agents on the survival and
reproduction of genetic individuals (genotypes) along with the specific phenotypes they express in
the course of some finite time period (e.g., one year) or per generation. As some genotypes show
reduced survival and/or reproduction relative to others, the gene pool will gradually change in the
direction of increasing population adaptation to the local environment. In other words, the alleles
and phenotypic trait values associated with the most fit individuals will increase in frequency over
time. This means that the population to the right in Figure 1 should be better adapted to the local
environment than the population we began with (to the left in Figure 1). This is a relative concept of
adaptation as an explicit organismal trait and will be discussed later.
Note that there are several difficulties with the simplified model of adaptive evolution in Figure 1.
Because adaptation is a continuous, ongoing process, there is no obvious beginning or end.
Population gene pools are shaped continually by agents of selection whose action is highly variable
in space and time (Bell 2010, Siepielski et al. 2013). Spatial heterogeneity in abiotic and biotic factors
will impact the members of a population in different ways and influence the scale at which
adaptation occurs (Richardson et al. 2014). Chance events, such as a seed dispersed to a high-
nutrient patch in a field, can result in an individual opportunistically growing to a larger size and
producing many more offspring than it would have, had it originally dispersed into a low-nutrient
patch despite what genotype it is. Such heterogeneity virtually assures that the adaptive process will
never reach an end point where all individuals are exquisitely adapted to a particular habitat
(Brandon 1990; Nesse 2005).
At the beginning of the sequence in Figure 1, it was assumed that the population was not well
adapted to the local environment. However, this is only true relative to the population at the end of
the sequence which is better adapted to a different local environment. Individuals in the initial
population must have been adapted to the local environment to some extent, otherwise they could
not be living there in the first place. Therefore, the sequence (Figure 1) strongly implies that

Mutation
Differential reproduction
Gene flow • •

• • •

Variable Selection episodes

gene pool
[Sexual reproduction] Less variable
gene pool

Mortality [differential survival] ADAPTATION [individuals

with greater ability to survive &

reproduce relative to previous

gene pools]

Figure 1. General model for adaptation as an ongoing population process driven by natural selection.
4 G. P. CHEPLICK

environmental changes are driving the episodes of selection and that there is a shift in adaptation in
progressing from the earlier to the later population. The relative nature of adaptation is not often
appreciated by educators using the term to depict a natural population-level process.
These considerations make it difficult to study adaptation as a microevolutionary process
occurring on ecological time scales (Phillips 2005; Hendry 2013, 2017) and questions on the relative
prevalence and strength of adaptation have been debated (Hendry and Gonzalez 2008). Ecological
approaches such as reciprocal transplant or common garden experiments that demonstrate a fitness
advantage to a population in its home habitat reveal the results of adaptive evolution generated by
a suite of selection agents acting on earlier generations (Cheplick 2015; Franks, Hamann, and Weis
2018). Details of the specific causative agents of selection responsible for adaptation are often not
known (MacColl 2011; Wadgymar et al. 2017). Molecular approaches that use genetic markers can
reveal the signature of adaptation in terms of DNA sequences and variants in candidate genes that
correlate with putative selection pressures such as climate factors (Franks and Hoffmann 2012;
Rellstab et al. 2016; Sork 2018; Wright et al. 2018). These molecular adaptations may be present in
some populations but not others; however, again they are the result of different selection agents
acting on populations repeatedly over multiple, unknown numbers of generations.

Evolutionary or ecological adaptation?

Adaptation as a biological concept should be taught as a continuous process common to all
populations and as an invaluable concept in ecology and evolutionary biology. Evolutionary
processes occur in an ecological setting and the agents of selection are environmental factors
(Brandon 1990; Cheplick 2015). It is not useful to distinguish ecological from evolutionary adapta-
tion. The latter phrase is actually redundant as biological adaptation developed historically as an
evolutionary concept (Amundson 1996). In alignment with the widely used phrase ecological
speciation in which barriers to gene flow arise between populations ‘as a result of ecologically
based divergent selection between environments’ (Nosil 2012, 7), one can use the phrase ecological
adaptation to depict a process of adaptive evolution that results from selection pressures that are
abiotic and biotic factors in the natural environment.
The domains of evolution and ecology should include the many agents of natural selection acting to
guide the microevolution of all populations and the ongoing process of adaptation (MacColl 2011;
Cheplick 2015; Wadgymar et al. 2017). As described next, the traits that result from adaptive evolution
are also called adaptations; they represent ‘a compromise among all the different biotic and abiotic
aspects of the environment that are the sources of natural selection’ (Reznick and Travis 1996, 282).

Adaptation as a trait
The process of adaptive evolution, by definition, must result in the generation of adaptive traits. An
adaptation then is typically denoted as any trait that ‘increases an organism’s fitness relative to
individuals lacking it’ (Herron and Freeman 2014, 78). The difficulty with this widely used, standard
textbook definition is that it implies that a particular trait is either present or absent, a dichotomy
that rarely occurs in nature. As noted by Stern (1970), the ‘all or none’ concept of adaptation limits
its usefulness in understanding the process of adaptive evolution.
Similar to Darwinian fitness, adaptation is probably best viewed as a relative concept (Stern 1970;
Brandon 1990; Reeve and Sherman 1993). There are several ways this relativity can be evident. In the
previous section, adaptive traits arose following successive episodes of natural selection and indivi-
duals became better adapted to the local environment relative to a variable population of individuals
earlier in the sequence (Figure 1). Therefore, a greater proportion of individuals in the adapted
population possess the phenotypic traits (adaptations) that improve survival and reproductive fitness
compared to the earlier population. This microevolutionary perspective on adaptation as an end point
 JOURNAL OF BIOLOGICAL EDUCATION 5

in a temporal sequence is difficult to use in practice because the phenotypic composition of the earlier,
non-adapted population is typically unknown (Blanquart and Gandon 2013).
The resurrection approach to understanding contemporary evolution, in which ancestral organ-
isms from the past are revived from stored propagules and compared with descendents under
common conditions (reviewed by Franks, Hamann, and Weis 2018), offers one technique to
examine adaptive evolution over short time scales (Kuester et al. 2016). This is because
a resurrection study involves a time-shift experiment (Blanquart and Gandon 2013) in which the
average fitness of a trait in a population can be compared across past and contemporary environ-
ments. Information on comparative variation in phenotypic and molecular genetic traits can then
be used to document changes in the phenotypic and genotypic composition of a population as it
adapts to a changing environment (Franks, Hamann, and Weis 2018). As Orsini et al. (2013, 274)
noted, dormant propagules ‘are convenient natural archives of population histories from which to
trace adaptive trajectories along extended time periods.’ Although a resurrection experiment does
not often reveal the agents of selection responsible for adaptive changes and the average temporal
separation between ancestors and descendents is only about 20 years in the experiments reviewed
by Franks, Hamann, and Weis (2018), this is clearly enough time to witness contemporary adaptive
evolution (Reznick and Ghalambor 2001; Carroll et al. 2007; Hendry 2017).
A second way adaptation can be viewed as relative occurs when a phenotypically variable
population is considered at a single point in time. If we assume a constant, homogeneous set of
environmental conditions and there is variation in relative fitness within the population, we can
reason that individuals with greater fitness are better adapted to that environment compared to
other individuals with lower fitness. In other terminology, the former show greater adaptedness to
the environment (Dobzhansky 1970; Endler 1986; Brandon 1990; Amundson 1996). The pheno-
typic traits associated with high relative fitness represent adaptations for the genotypes that possess
them compared to less-fit genotypes without the traits (or more likely, with different phenotypic
values if they are quantitative traits). Note that this is adaptation at the level of the individual rather
than the population-level adaptation described in the previous paragraph.

Adaptive value and adaptive significance: an example

In choosing an example of the adaptive value of a phenotypic trait, it is important to select a simple
trait that is easy to quantify, shows variation among individuals, and that is likely to be correlated
with reproductive fitness. It also helps if there is a simple hypothesis regarding the adaptive value of
the trait that is directly related to conditions of the natural environment. Here I consider leaf
pubescence, a quantitative trait that shows phenotypic variation in a plant population in an arid
environment.
A trait that is important for plants in warm, dry conditions is especially timely because it
illustrates how a population could adapt during microevolution in response to the warmer, drier
conditions expected to develop in more regions as global climate changes (Briggs 2009). Indeed,
rapid rates of phenotypic evolution and adaptation over short time frames have been described for
plants in relation to anthropomorphic factors (Rieseberg 2017), so plants can provide a realistic
scenario for rapid adaptive evolution. A plant trait is also useful for instructive reasons, because
students should be less likely to fall into the teleological trap in attempting to explain adaptation
(Gregory 2009) because attributing adaptive responses to the environment as purpose-driven will
be difficult for organisms that lack a central nervous system and are unable to think!
For the example, assume that plants with the most pubescent leaves lose the least water by
evapotranspiration (Ehleringer and Mooney 1978; Housman, Price, and Redak 2002) and conse-
quently show greater photosynthesis and growth, thereby producing more seeds, compared to
plants with lower densities of pubescence. This supports the hypothesis that leaf pubescence
represents an adaptation to arid conditions, even though no plants are completely devoid of leaf
hairs. Thus, the adaptation could be best characterised as a subset of the possible range of variation
6 G. P. CHEPLICK

in leaf pubescence within the population that includes the greatest densities of leaf hairs in
individuals with high fitness. The relative nature of adaptation is clear in this example: there is
no line separating individuals with high versus low fitness. If leaves of all individuals have at least
some pubescence, then leaf pubescence might be considered adaptive for all individuals, but to have
greater adaptive value in a dry habitat for individuals in which hairiness is well developed.
The extent of the fitness advantage imparted by possession of an adaptive trait compared to those
without the trait (or with different quantitative values of the trait) can be a measure of the adaptive
value of the trait. Obviously, the trait that improves relative fitness greatly has greater adaptive value
than phenotypic variations of the same trait that only improve fitness to a minor extent. Because
a phenotypic trait is only part of a complex set of ‘developmentally correlated characters’
(Dobzhansky 1956, 340), an adaptive trait may be difficult to isolate in relation to the genetic,
physiological, and developmental factors that affect it (West-Eberhard 2003).
Whereas adaptive value designates the magnitude of the benefit (improved fitness) of a specific
phenotypic trait in relation to the environment, the phrase adaptive significance specifies the explicit
functional importance of a phenotypic trait to relative fitness in relation to selective pressures of the
environment. The adaptive significance of leaf pubescence to plants is to reduce evapotranspira-
tional loss of water, increase photosynthetic efficiency, and improve the individual’s chance of
surviving and reproducing under arid conditions (Ehleringer and Mooney 1978; Meinzer and
Goldstein 1985; Housman, Price, and Redak 2002). Although the functional, adaptive significance
of a single trait is never easy to demonstrate (Williams 1966; Mayr 1983; Reznick and Ghalambor
2001; Phillips 2005), evolutionary hypotheses can be tested experimentally (Wadgymar et al. 2017).
If dry conditions have functioned, during the process of adaptation, as the selective driver for the
evolution of greater leaf pubescence, then populations should show genetically based differences in
the extent of pubescence that can be positively related to the aridity of the sites in which they occur.
The phenotypic expression of the trait can be measured on multiple populations grown in one or
more common gardens (Sandquist and Ehleringer 1997; Housman, Price, and Redak 2002): if
aridity of the site of origin is positively related to the degree of leaf pubescence in the populations
and differences are maintained in the garden (Figure 2(a)), then there is a good chance that
populations have differentiated in leaf pubescence as an adaptive response to the dryness of soils
in their habitats. This is not an unreasonable supposition because genes that determine hairs on
plants have been identified (Wright et al. 1999; Kärkkäinen and Ågren 2002; Kivimäki et al. 2007).
Also artificial selection experiments, powerful tools for understanding adaptation (Conner 2003),
have successfully changed the extent of hairiness of plant organs (Vasek 1986; Ågren and Schemske
1992, 1994). In nature there could be significant variation in the positive relationship of leaf
pubescence to aridity because it is unlikely that habitats are consistently dry or moist from
one year to the next and thus selection pressures will vary over time (Siepielski, DiBattista, and
Carlson 2009) and furthermore, leaf hairs can have other adaptive functions such as the deterrence
of herbivory (Johnson 1975; Kivimäki et al. 2007).
A third piece of evidence is needed to demonstrate the adaptive value of a phenotypic trait:
a positive relationship of some measure of relative fitness to quantitative values of the trait that has
presumably been under selection (Lande and Arnold 1983; Endler 1986; Conner and Hartl 2004).
We might grow individuals representing genotypes that vary in their level of leaf pubescence in an
arid habitat (or expose them to experimental drought or other treatments; e.g., Roy, Stanton, and
Eppley 1999) and record a measure of reproductive fitness such as fruit or seed production. If
individuals with hairier leaves show greater fitness under dry conditions than those individuals with
fewer leaf hairs (Figure 2(b)) but no real advantage under moist conditions, then it can be inferred
that aridity is a selection pressure likely to select for genotypes that make hairier leaves, thereby
reducing transpirational water loss and increasing photosynthetic efficiency (Ehleringer and
Mooney 1978; Kärkkäinen, Løe, and Ågren 2004).
To conclude, are we justified in referring to the phenotypic trait leaf pubescence as an ecological
adaptation of our study species to arid environments? We are, only if we had compared genotypes
 JOURNAL OF BIOLOGICAL EDUCATION 7

Figure 2. Demonstrating the adaptive significance of a quantitative phenotypic trait (leaf pubescence) in a hypothetical plant
species that typically grows in sites that vary in aridity. (a) Results of a common garden experiment in which mean leaf
pubescence of a population increases with increasing aridity of the site where the population normally grows (that is, its site of
origin). (b) Results of an experiment showing that individuals (genotypes) with greater leaf pubescence show higher relative
fitness in a dry environment.

with pubescent leaves to genotypes that are completely hairless (glabrous), as has been done for
Arabidopsis lyrata in relation to herbivore pressure (Kivimäki et al. 2007). This would satisfy the
requirements of the traditional definition of adaptation as any trait that increases an organism’s
fitness relative to individuals lacking it (Herron and Freeman 2014). However, if all individuals in
populations of our species show some level of pubescence that varies in a quantitative way among
genotypes, as demonstrated for hair density in A. lyrata (Kärkkäinen and Ågren 2002) and Sinapis
(formerly Brassica) arvensis (Roy, Stanton, and Eppley 1999), but none are completely hairless, then
hairier leaves have adaptive value when conditions are dry. Nonetheless, leaf pubescence may not
necessarily have any adaptive value when the environment is mesic, so referring to this trait as
a species-level adaptation to arid habitats is misleading.
8 G. P. CHEPLICK

Levels of adaptation
In the leaf pubescence example, use of adaptation to describe this trait was not applicable at the
species level because there could be specific habitats within the species’ range in which there would
be no fitness benefit to possessing hairy leaves. Historically, adaptation, when used to describe
a trait, has been applied to different levels in the biological hierarchy from individuals to popula-
tions to species (Stern 1970; Munson 1971) and to different levels of the developmental hierarchy
from molecules to phenotypic traits (West Eberhard 2003; Griffiths and Gray 2004).
Pubescent leaves can be viewed as an adaptation to high herbivory in some populations of
A. lyrata, while other populations produce leaves that are completely hairless (Kärkkäinen, Løe,
and Ågren 2004). In this species in which the pubescent vs. hairless traits are controlled by
alternative alleles at a single locus (Kärkkäinen and Ågren 2002), directional selection exerted by
insect herbivores will favour the adaptive evolution of pubescence in populations where herbivore
presence is consistent over time. This population-level designation of the term adaptation is what is
typically meant when ‘local adaptation’ is investigated for phenotypic traits with reciprocal trans-
plant experiments (Kawecki and Ebert 2004; Leimu and Fischer 2008; Cheplick 2015). This is also
true for local adaptation examined at the molecular genetic level (Savolainen, Lascoux, and Merilä
2013; Tiffin and Ross-Ibarra 2014).
But what about adaptation at the level of individual genotypes? Stern (1970) distinguished
‘adaptation at the level of the individual’ from ‘adaptation of the population’ in a review written
about 50 years ago. If the population on the right in Figure 1 is adapted to its local habitat, then it
follows that the individuals that comprise it are also adapted to their habitat. Although an individual
that survives to produce more descendents than other individuals in a population may be said to
possess adaptive traits, these adaptations are likely to be manifest as specific phenotypic values for
quantitative traits (e.g., leaf pubescence) that vary among individuals. Hence, adaptation in this
context is a completely relative term and further, at the individual level, it does not differ function-
ally from the concept of relative fitness. Individuals differ in the extent to which they exhibit
adaptive traits, which act to improve fitness in a particular environment (Stern 1970). Finally, it
should be recalled that the reason individuals show adaptation to the present environment is
because populations in the past had experienced similiar environmental conditions (Figure 1)
that functioned as selection pressures guiding the process of adaptive evolution.

Exaptation, ‘pre-adaptation’, and maladaptation: useful terms?

The term pre-adaptation has long been used to denote a trait that no longer provides the original
function for which it evolved, but has instead been selected for some new function; thus, the former
trait is said to be ‘pre-adapted for a new function’ (Bock 1959, 201). Of course, this term undermines
the process of adaptive evolution, for how can there be any type of ‘adaptation’ in anticipation of
selection pressures in a future environment? The fact that some organisms possess traits evolved in
relation to one habitat that allow them to be evolutionarily successful in other habitats (e.g., invasive
species, Mack 2003; Guo et al. 2014), is probably fortuitous and may have little to do with the
original adaptive value of those traits. Although the general idea of pre-adaptation could have some
heuristic value in teaching traits as adaptations, it is probably best avoided because it does not reflect
adaptive evolution.
Gould and Vrba (1982) famously introduced the term exaptation for traits evolved in the past for
some function for which they are no longer used; rather, the traits have since evolved new functions in
response to different selection pressures. They hoped that exaptation would eliminate use of the
teleological, ‘fatally flawed’ term ‘pre-adaptation’ (Gould 2002, 1232). However, because most traits
are likely to have been modified from pre-existing versions of those same traits that may have been
used in a way that differs from their current use, all adaptations might be said to be exaptations,
making the latter term redundant (Reeve and Sherman 1993; Larson et al. 2013). For example, leaf
 JOURNAL OF BIOLOGICAL EDUCATION 9

pubescence that initially evolved to function in reducing surface temperatures and evapotranspiration
is an adaptation and an exaptation (if its origin cannot be ascribed to natural selection, but which has
now been co-opted for a current use; Gould 2002). It is also an exaptation if the new function of
herbivore deterrence arises from a different selective agent (herbivores). Whether or not the origin of
leaf pubescence involved specific selection pressures, it could still be described as an exaptation.
Larson et al. (2013) speculated that the failure of exaptation to gain a foothold in evolutionary biology
has likely resulted from lack of a formal definition that distinguishes it from adaptation.
Because the fit between individuals and their natural environment is seldom perfect (Seger and
Stubblefield 1996), most genotypes and populations can be expected to be incompletely adapted to
some extent because ‘optimal’ conditions needed for the greatest fitness are rare in nature (Cheplick
1991). Recognition of the inefficiency of adaptive evolution should enable educators and students to
reject the notion of traits that function as perfect adaptations to the local environment. Therefore,
because many factors can constrain the development of local adaptation, populations may often
show maladaptation (Crespi 2000; Thompson, Nuismer, and Gomulkiewicz 2002; Nesse 2005;
Hendry and Gonzalez 2008; Brady et al. 2019). There are many possible causes of maladaptation,
including mutations, genetic drift, gene flow, and lack of sufficient genetic variation (Crespi 2000;
Brady et al. 2019). Maladaptation is conceptualised as a set of phenotypes that do not exhibit the
maximum relative fitness achievable in a particular environment (Crespi 2000; Hendry and
Gonzalez 2008). Thus the phenotypic traits exhibited are maladapted to the local environment.
Examples of maladaptation can be found in articles collected in a special issue of Evolutionary
Applications, Volume 12 (2019). In reciprocal transplant experiments, populations in their local site
are sometimes outperformed by populations from foreign sites (Kawecki and Ebert 2004; Garrido
et al. 2012; Vesakoski and Jormalainen 2013; Cheplick 2015). When this occurs, one is tempted to
state that the local population must be maladapted compared to the foreign population. However,
the ‘optimal’ phenotypic values that will maximise fitness for a particular genotype are difficult to
determine and environmental conditions will often constrain the extent to which this optimum can
be achieved (Cheplick 1991). It is likewise a challenge at the population level to quantify ‘relative
fitness maladaptation’ which is defined as ‘the difference between observed mean fitness and the
mean fitness of a comparable population at the local optimum’ (Hendry and Gonzalez 2008, 693).
The usefulness of maladaptation as a descriptive term for an evolutionary process is not great
because it can be applied to every step along the way to adaptation in Figure 1; however, maladapted
traits may be applied to those phenotypes or populations in which quantitative (or qualitative)
values for these traits are not the values that would provide the greatest relative fitness in a specific
environment (if these trait values can be objectively defined).

Educational implications
Adaptation can be taught as a corollary to the precepts of natural selection found in most textbooks
on evolution. An excellent exposition on natural selection and common misconceptions associated
with it can be found in Gregory (2009). The statements below are guided by Herron and Freeman’s
(2014, 77) basic description of natural selection.

(1) Individuals in a population differ from one another. These differences are phenotypic, but
may have some underlying genetic basis.
(2) The differences among individuals are, at least to some extent, passed from parents to
offspring. That is, because there is some genetic basis to the phenotypic differences, they
are heritable.
(3) Some individuals are more successful at surviving and reproducing than others.
(4) The individuals in precept (3) are more successful because of the particular traits they have
inherited and they will then pass the genes/alleles for these phenotypic traits on to their
offspring.
10 G. P. CHEPLICK

The result is that, if the four precepts hold over time (i.e., natural selection occurs continually), the
individuals in the population will gradually possess phenotypes better suited for survival and
reproduction. In other words:

(5) Continued success of the individuals in precept (4) will eventually result in future descen-
dents, and the population they are part of, showing adaptation to the local environment.

Once students understand that individual fitness is based on survival and reproduction relative to
other individuals in a population in a particular environment, it can be readily visualised that
adaptive traits are also possessed by individuals and will show quantifiable differences among the
members of a population. This is true whether a trait is phenotypic, that is, a measurable,
quantitative morphological characteristic such as leaf pubescence in the example described earlier
(Figure 2), or molecular, that is, a DNA or protein variant of a candidate gene locus that has
adaptive value in a particular environment (Cheplick 2015; Pardo-Diaz, Salazar, and Jiggins
2015). Collectively, the individual phenotypes may comprise a population better adapted to the
local environment when compared to some other reference population either earlier in the
temporal sequence (Figure 1) or inhabiting a similar environment. It must be emphasised that
only a variable population can evolve and undergo the process of adaptation as guided by natural
selection. Although there are envisioned mechanisms besides natural selection that might result
in adaptive evolution (West-Eberhard 2003: Kull 2014), a firm grounding in the precepts of
natural selection is necessary for students to grasp the complex concept of adaptation without
recourse to teleological explanations (Kampourakis and Zogza 2008; Gregory 2009; Blancke et al.
2014). Although exaptation and maladaptation have some utility in describing how already-
evolved traits may be co-opted by selection for other functions or how adaptive evolution, as on
ongoing process, does not invariably result in a perfect fit of organism to environment, the term
pre-adaptation is probably best avoided because it does not reflect adaptive evolution.

Conclusions
The phrase ecological adaptation can be used to denote both an evolutionary process and
a phenotypic or molecular trait variant that results from that process. The process occurs at the
population level in nature and is guided/shaped by environmental factors, abiotic and biotic, that
are the agents of natural selection. Like the population being presented as a central concept to
ecology (Berryman 2002), ecological adaptation is a central concept to evolutionary biology. Note
that a failure to apply ‘population thinking’ can lead to problems in students’ understanding of
natural selection and adaptation (Cooper 2017). As a process, it should be emphasised to students
that ecological adaptation does not require a long time and there are now many examples of
contemporary adaptive evolution (Reznick and Ghalambor 2001; Carroll et al. 2007; Hendry 2017;
Reznick, Losos, and Travis 2019).
Continuous variation in phenotypic as well as molecular traits is best viewed as spread along
a continuum of fitness consequences in a naturally variable environment (with correspondingly
variable agents and strengths of selection). It is the interaction of individual phenotypes (and their
genotypes) with environmental factors that determine whether a trait is adaptive or possibly
maladaptive. All are not equal in terms of adaptation which is a relative concept (Reeve and
Sherman 1993), whether considered among individuals within a single population or among
populations within a species’ range. Ecological adaptations should not be viewed as depicting
a perfect fit between organism and environment, but only as a better fit for some individuals and
populations relative to others, as evidenced by their individual fitness and mean fitness among
individuals in a population, respectively. Any organism able to survive and reproduce in a given
environment must be adapted to it to some extent whenever population gene pools in the past have
been exposed to the same types of selection agents that currently occur. The legacy of adaptation as
 JOURNAL OF BIOLOGICAL EDUCATION 11

a process must be the adaptive value of the phenotypic and molecular trait variants found in
individuals and populations living in the current environment.

Acknowledgments
Thanks are extended to J. F. Scheepens and an anonymous reviewer for providing detailed comments and suggestions
on an earlier version of the manuscript.

Disclosure Statement
No potential conflict of interest was reported by the author.

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