REVIEW ARTICLE

PUBLISHED: 21 FEBRUARY 2017 | VOLUME: 1 | ARTICLE NUMBER: 0065

Human behaviour as a long-term ecological driver

of non-human evolution
Alexis P. Sullivan1, Douglas W. Bird2 and George H. Perry1,2,3*
Due to our intensive subsistence and habitat-modification strategies—including broad-spectrum harvesting and predation,
widespread landscape burning, settlement construction, and translocation of other species—humans have major roles as eco-
logical actors who influence fundamental trophic interactions. Here we review how the long-term history of human–­environment
interaction has shaped the evolutionary biology of diverse non-human, non-domesticated species. Clear examples of anthro-
pogenic effects on non-human morphological evolution have been documented in modern studies of substantial changes to
body size or other major traits in terrestrial and aquatic vertebrates, invertebrates, and plants in response to selective human
harvesting, urbanized habitats, and human-mediated translocation. Meanwhile, archaeological records of harvested marine
invertebrates and terrestrial vertebrates suggest that similar processes extend considerably into prehistory, perhaps to
50,000 yr bp or earlier. These results are consistent with palaeoenvironmental and other records that demonstrate long-term
human habitat modification and intensive harvesting practices. Thus, while considerable attention has been focused on recent
human impacts on ‘natural’ habitats, integrated evidence from modern biology and archaeology suggests a deep history of
human entanglement with our ecosystems including substantial effects on the evolutionary biology of non-human taxa. The
number and magnitude of such effects will probably increase given the continued intensification of anthropogenic activities and
ecosystem impacts, including climate change and direct genetic modification.

T
he subsistence and habitat-modifying behaviours that typify
how humans interact with their surrounding environments
have broad and temporally profound effects on natural eco­
systems1. At local levels, co-evolutionary relationships between
small-scale human societies and non-human taxa in the same com-
munity can be so longstanding and immersive that the removal of
humans results in simplified food webs or ecosystem collapse2,3,
while in the context of global population growth the intensity of
human–environment interactions has led to numerous docu-
mented cases of wildlife population decline and extinction4,5. Given
the extent and rate that human-mediated climate change and other
by-products of increasing human population density are predicted
to impact future ecosystems6,7, these issues are of major concern to
biologists, ecological anthropologists, and policymakers.
In addition to ecosystem health and wildlife extinction risk,
human behaviour also influences the evolutionary biology of non-
human species. Extensive morphological evolution mediated by
human behaviour has been thoroughly documented for domesti-
cated plants and animals8,9, but these processes are in fact consider-
ably more widespread, extending to non-domesticated species. That
is, wild populations of non-human taxa can adapt via natural selec-
tion on functional genetic variation in response to human-induced
ecological changes10. In some cases, these morphological and behav-
ioural adaptations may help certain species avoid extinction. These
processes could have cascading effects on ecosystem function6,11, so
they are an important factor to consider in the broader context of
human–environment interactions.
Clear examples of anthropogenic effects on the evolutionary
biology of non-human, non-domesticated species have been docu-
mented in modern studies of body size or other morphological trait
change in response to selective human harvesting of natural popu-
lations of vertebrates, invertebrates, and plants11–13. Analyses of the
archaeological record suggest that these processes likely extend con-
siderably into prehistory 14, perhaps even to earlier than 50,000 yr bp
(years before present), and mediated by Neandertals15 in addition
to anatomically modern humans. Non-human evolutionary adap-
tations to human-mediated ecological changes are also not limited
to direct harvesting pressure effects. For example, human land-
scape modification practices, which predate the onset of agriculture
~12,000 yr bp and have since then intensified1, may too be catalysts
for natural selection in affected non-human taxa6,16.
In this Review we describe potential mechanisms for non-human
adaptive evolution in response to human behaviour, with human
behaviour defined broadly to encompass landscape modification
(including niche construction); the harvesting, artificial selec-
tion, or translocation of non-human species; and even current and
potential future directed practices involving genetic modification
and de-extinction. These processes are illustrated by examples from
modern evolutionary biology and enhanced with ethnographic
and prehistoric perspectives that include discussion of evidence
for the long-term history of anthropogenic effects on the environ-
ment. We focus primarily on morphological evolution, which does
not encompass all adaptations (for example, genetically mediated
behavioural or metabolic adaptations) but provides opportunities
for insights from modern biology to be translated to the archaeo-
logical and palaeontological records. The consideration of these
data in a long-term, integrated framework will ultimately help us
identify and model these evolutionary processes as they may occur
in the future.
The antiquity of humans as trophic regulators
Disturbance ecology quantifies the effects of natural ecosystem dis-
ruptions that may result from abiotic forces (for example, fire, flood
and drought) or biotic variation (for example, intensive predation,

1
Department of Biology, Pennsylvania State University, University Park, Pennsylvania 16802, USA.2Department of Anthropology, Pennsylvania State
University, University Park, Pennsylvania 16802, USA. 3Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, Pennsylvania
16802, USA. *e-mail: ghp3@psu.edu

NATURE ECOLOGY & EVOLUTION 1, 0065 (2017) | DOI: 10.1038/s41559-016-0065 | www.nature.com/natecolevol 1

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REVIEW ARTICLE NATURE ECOLOGY & EVOLUTION

disease outbreak and depletion of keystone species)17. Humans have
major roles as biotic influencers of ecological disturbance due to
our intensive subsistence strategies that include broad-spectrum (of
a high diversity of resources) harvesting and predation18–20, wide-
spread landscape burning practices21–24, and habitat modification
for agriculture, aquaculture, and shelter 25. In fact, the term ‘hyper-
keystone species’ has recently been coined to describe humans, as
our subsistence behaviours in a given habitat impact multiple other
keystone species, with extensive resultant ecosystem effects26.
Although many studies of the relationships between human
activity and the population health and evolution of non-human spe-
cies have focused on recent human impacts in ‘natural’ eco­systems,
archaeological and palaeoenvironmental records demonstrate a
long-term history of major anthropogenic effects that began well
prior to the origins of agriculture1.
With respect to intensive harvesting, while there is fossil-record
evidence for the consumption of meat by African hominins by at least
2.5 million yr bp27,28, it is unclear whether this early record reflects
hunting or scavenging and whether this behaviour was intense or
sporadic29. However, good evidence for repeated, systematic butch-
ery of terrestrial vertebrate species by hominins, consistent with tar-
geted hunting and processing, is observed by ~780,000 yr bp30, and
hafted spear technology appears in the archaeological record by at
least ~500,000 yr bp31. Archaeological data from South Africa32 and
Spain33 also show that broad use of coastal resources by hominin
foragers began by at least 150,000 yr bp34.
Analyses of pollen and charcoal records suggest the initiation
of widespread anthropogenic landscape burning between ~50,000
and 40,000 yr bp in Borneo and New Guinea, coincident with the
respective appearances of modern humans in each region35,36. Some
scholars even infer that the purposeful use of fire for habitat mod-
ification—a practice common to both agriculturalists and hunter-
gatherers worldwide today 23,24—may have roots in the evolution of
the genus Homo close to two million yr bp21.
Human–environment interactions later intensified further with
the origins and spread of agriculture and animal husbandry begin-
ning ~12,000  yr  bp1. Human-mediated ecological impacts during
this period have included extensive land clearing, terracing, water-
way diversion, the construction of permanent settlements and ulti-
mately urban centres, translocation of non-endemic species to new
habitats, the potential for magnified selective hunting and fishing
pressures on non-domesticated species associated with increasing
human population sizes and densities, climate change, and now
even direct genetic modification of non-human taxa.
Through these various processes humans became deeply entan-
gled in their ecosystems, as illustrated by the cascading effects that
have been observed following the removal of human activity from
some habitats3. For example, in desert Australia, Aboriginal predation
of monitor lizards involves disturbing climax vegetation via burning
tracts of old-growth xeric grassland, creating a tight mosaic of veg-
etative succession that supports higher densities of many tradition-
ally hunted species37,38. A mid-twentieth-century hiatus in traditional
burning led to trophic collapse and coincided with the extinction of
at least 21 endemic marsupials2. Thus, while human predation and
habitat modification can certainly affect non-human population
distributions negatively, leading to extinction and food web simpli-
fication5,39,40, there is also strong evidence for significant ecological
adaptation to the long-term keystone presence of intensive human
disturbance, which could include adaptive morphological evolution
in non-human taxa.
Human behaviour as a driver of non-human evolution
One of our goals in this Review is to demonstrate the antiquity of
widespread phenotypic adaptation to human behaviour by connect-
ing observations and insights from modern evolutionary biology
to archaeological and palaeontological observations. To do so, we
focus on the evolution of major morphological phenotypes—that is,
traits that may be preserved in prehistoric records (unlike, for exam-
ple, behavioural and metabolic changes)—as one subset of a diverse
spectrum of genetic-based traits in non-human species that have
evolved in response to human behaviour 41–44. For the same reason
we also do not discuss bacteria, parasites, and other micro­organisms
whose evolutionary biology is also affected by humans45–48. However,
to the extent that human behaviour is a long-term driver of macro-
scale morphological change in non-human plants and animals,
we would expect these processes to have probably affected the
evolutionary histories of other phenotypes and organisms as well.
Artificial selection associated with the domestication of non-
human animals and plants is the best-known example of mor-
phological evolution in response to human behaviour. While
agriculture and pastoralism originated by at least ~12,000  yr  bp1,
the roots of these processes likely extend considerably further into
prehistory, for example to ~23,000 yr bp49 or earlier 50 for plants and
>30,000 yr bp for dogs51. Here, because both the scale and archaeo-
logical prehistory of morphological evolution in domesticated taxa
have been reviewed extensively 8,9,52–54, we will instead focus our
discussion on four other mechanisms by which human behaviours
could be ecological drivers of morphological evolution: (i) size- or
trait-selective harvesting; (ii) landscape modification and urbani-
zation; (iii) human-mediated ecosystem taxonomic turnover; and
(iv) looking towards the future, climate change and direct genetic
modification (Fig. 1).
Response to size- or trait-selective harvesting pressures
Human patterns of prey selection can vary substantially from those
of other predators. Although probably not applicable to all socie-
ties, at least some human populations may harvest particular spe-
cies with unparalleled intensity, and may disproportionately target
large adults of a given prey species or individuals with a specific tro-
phy feature, such as antlers or horns18. Rapid phenotypic evolution
may result 11.
Morphological evolution has been especially well documented in
fisheries, in which larger prey are typically of higher value and netting
technology may greatly enrich the catch for larger individuals based
on the sizes of the net openings13,55–57. Body length and mass reduc-
tions of 25% or greater have been documented over time periods of
only one or several decades in multiple independent taxa58–61.
In addition to marine and freshwater vertebrates, organism size
changes in response to human harvesting pressures have also been
reported in natural populations of terrestrial vertebrates and even
plants (Fig. 2). An excellent example, documented in a carefully con-
trolled study, is that of the wild snow lotus Saussurea laniceps. This
plant, from the eastern Himalayas, is used in traditional Tibetan and
Chinese medicine for headache and high blood pressure treatments.
Larger plants are considered more potent and thus collected prefer-
entially. Based on herbarium specimens (of flowering plants; when
maximum plant height is achieved), Law and Salick62 reported a
~45% decrease in S. laniceps heights over the past century. In contrast,
flowering heights of the sympatric and related—but substantially
less desired medicinally and little harvested—snow lotus Saussurea
medusa were unchanged over the same period. Moreover, modern
S. laniceps individuals subject to harvesting in non-protected areas
were ~70% shorter than those in protected areas62.
Trophy hunters exert directional pressure on a particular
pheno­ type, potentially leading to the evolution of smaller fea-
tures across the population or higher rates of feature absence. For
example, illegal ivory hunting in Zambia resulted in an increase of
>300% (from 10.5% to 38.2%) of tuskless female African elephants
(Loxodonta africana) from 1969 to 198963. Trophy hunting may also
have pleiotropic effects on other phenotypes that are not the direct
targets of selection, as observed for bighorn sheep (Ovis canadensis)
on Ram Mountain in Alberta, Canada. Specifically, in addition to a

2 NATURE ECOLOGY & EVOLUTION 1, 0065 (2017) | DOI: 10.1038/s41559-016-0065 | www.nature.com/natecolevol

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NATURE ECOLOGY & EVOLUTION REVIEW ARTICLE
Human behaviour or impact Non-human morphological evolution examples

Trophy feature
reduction
Harvesting
pressure
Body size
reduction

Wing shape
changes
Landscape
modification
Altered limb
proportions

Limited gape for

toxic prey avoidance
Translocation
and extinction
Smaller fruits
and seeds

Increased
seed size
Domestication
Reduced horn
and body size

Accelerated
1 year 1 year growth rate
Genetic
modification
De-extinction?

Figure 1 | Model of how human behaviour may effect non-human morphological evolution.

~30% reduction in bighown male horn length over 23 years of horn-
size-focused hunting pressure (Fig.  3), body mass also decreased
~23.5% over the same period64,65.
Is trophy hunting limited or widespread among human societies,
and what is the antiquity of this behaviour? In many societies, pres-
tige goods do serve as costly signals of status and commitment and
probably play an important role in the development of inequality 66,67,
and in foraging groups hunting is commonly as much a political
activity as it is a provisioning practice68,69. Discerning archaeological
signatures of prestige hunting is difficult but has been proposed in
several cases70.
Well-documented archaeological evidence for prey size changes
in response to human harvesting pressure does exist in the record
of intertidal mollusc exploitation14 (Fig. 4). While many predators
(marine, terrestrial, and avian) exploit shellfish, only humans trans-
port large loads to central locales for repeated processing and depo-
sition, creating substantial heaps or trash ‘middens’ of the inedible,
durable mollusc shells and the remains of other taxa that come
to represent temporal records of both direct human predation on
these animals and their sizes71,72. Such harvesting can have substan-
tial effects, with selective pressures resulting in either morphologi-
cal change in targeted molluscs or predation resulting in shellfish
populations with persistently skewed age–size profiles.
Modern human intertidal foragers worldwide are selective and
highly sensitive to changes in the trade-offs associated with search-
ing for and handling different types and sizes of shellfish73–75. Because
shellfish are sessile or slow on-encounter, shell size predicts the
macro-nutritional return rate of molluscs, and correlates well with
ethnographic measurements of the probability that foragers will
select an individual encountered while foraging 76. Thus, observed
foraging behaviour suggests selective preferences for larger mol-
luscs, generating conditions that could lead to evolutionary size
decreases over time for species harvested intensely by humans.
These expectations are consistently met by analyses of the archae-
ological record. Early evidence for routine, large-scale intertidal
mollusc exploitation has been recorded beginning in the middle
stone age (~120,000 to 60,0000 yr bp) at coastal cave sites in South
Africa71,77. These South African middle stone age shellfish assem-
blages have been compared to those that accumulated in midden
layers dated to the later stone age (~12,000 to <1,000 yr bp), with sig-
nificant observed reductions over time in the sizes of all represented
species78,79, including for the Cape turban shell (Turbo sarmaticus)
as depicted in Fig. 5.
Similar evolutionary trends are evident in many coastal environ­
ments elsewhere. For example, molluscs recovered from mid-
den layers dated to ~19,000  to 9,000  yr  bp at Riparo Mochi, Italy

NATURE ECOLOGY & EVOLUTION 1, 0065 (2017) | DOI: 10.1038/s41559-016-0065 | www.nature.com/natecolevol 3

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REVIEW ARTICLE NATURE ECOLOGY & EVOLUTION

Human Affected Magnitude Evol. rate

Species Timeframe Ref.
activity phenotype of change (darwins)

African elephant 1969–1993

Female tusklessness +342% N/A 63
Loxodonta africana (24 years)
Bighorn sheep 1972–2002 Male horn length
–31% 12,126 64
Ovis canadensis (30 years) Male body mass

Wild reindeer 1969–1985

Body mass –13% 7,678 139
Rangifer tarandus (16 years)
American ginseng 1900–2000 Sympodium height
–26% 3,285 140
Panax quinquefolius (100 years) Root length
Himalayan snow lotus 1900–2000
Flowering height –44% 5,878 62
Saussurea laniceps (100 years)
Grayling 1903–1998
Body length –7% 719 141
Thymallus thymallus (95 years)
Pink salmon 1951–1975
Body mass –26% 13,143 58
Oncorhynchus gorbuscha (23 years)
Rock lobster 1972–2005
Carapace length –13% 4,071 142
Panulirus cygnus (33 years)
Red porgy 1979–1994
Fork length –12% 8,740 143
Pagrus pagrus (15 years)
Sheephead 1969–1998
Body mass –41% 18,018 60
Semicossyphus pulcher (29 years)
Sole 1960–2002
Body length –14% 3,588 144
Solea soleas (42 years)
Volcano keyhole limpet 1869–1981
Shell length –5% 425 138
Fissurella volcano (112 years)
Marine snail 1903–1985
Shell length –6% 762 138
Acanthinucella spirata (82 years)
House finch Present day
Beak length +2% N/A 94
Carpodacus mexicanus (urban vs rural)
Cliff swallow 1983–2012
Wing length –2% 800 87
Petrochelidon pyrrhonota (29 years)
Gray jay 1900–2008
Wing pointedness +28% 2,257 90
Perisoreus canadensis (108 years)
Anole lizard Present day Limb length
+2% N/A 93
Anolis cristatellus (urban vs rural) Subdigital scale number
Grasshopper Present day Body mass
+13% N/A 145
Chorthippus brunneus (urban vs rural) Relative wing length
Fence lizard Present day
Hindlimb length +3% N/A 109
Sceloporus undulatus (fire ant vs no fire ant)
Purple loosestrife Present day
Vegetative size –50% N/A 146
Lythrum salicaria (N vs S invasive range)
Soapberry bug 1925–2004
Mouthpart size +7% 946 147
Leptocoris tagalicus (79 years)
Palm seeds Present day
Seed size –16% N/A 129
Euterpe edulis (large fauna vs not)

Trophy Plant Magnitude of change (%)

Hunting
hunting harvesting
Net/trap Invertebrate ≥50 25 0 25 ≥50
Angling Evolutionary change per
fishing harvesting
million years (darwins)
Habitat modification/
Translocation Defaunation
urbanization
1 10 100 1,000 10,000+

Figure 2 | Selected modern examples of morphological change in response to human behaviour. The presented magnitudes of phenotypic change
represent approximate percentages of difference from earliest measured value. The reported evolutionary rates (in darwins)130 reflect the magnitude of
morphological change (absolute value of the difference between the natural log of the starting trait value and the natural log of the ending trait value) per
million years, for cases with available morphological trait measurements (which excludes the elephant presence/absence example) and information on the
number of years over which the change occurred. For cases in which multiple phenotypes were analyzed, the magnitude of change depicts the first listed
phenotype. Only one of multiple modern examples of these effects in different species of salmon59,61,137 and shellfish138 were included in the figure. Photo
credits (from top to bottom): Geoff Gallice; Gabriel Pigeon; US Fish and Wildlife Service, Jon Nickles; US Fish and Wildlife Serve Division of Public Affairs,
Dan J. Pittillo; ref. 62, PNAS; US Fish and Wildlife Service, Phil Coleman; Bering Land Bridge National Preserve; Gnangarra; SEFSC Pascagoula Laboratory,
Collection of Brandi Noble, NOAA/NMFS/SEFSC/NOAA Photo Library; US NOAA; Tvabutzku1234; Jerry Kirkhart; Scott Loarie; Ken Thomas; Ken Thomas;
Gavin Schaefer; Geoff Gallice; G.-U. Tolkiehn; Ken Thomas; AnRo0002; gailhampshire; Alex Popovkin, Bahia, Brazil.

4 NATURE ECOLOGY & EVOLUTION 1, 0065 (2017) | DOI: 10.1038/s41559-016-0065 | www.nature.com/natecolevol

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NATURE ECOLOGY & EVOLUTION REVIEW ARTICLE
a b
90
n = 22
n = 16 10–fold decline of sport
n = 16
harvest starting in 1996
Horn lengths (cm) of 4-year-old males

80 n = 34
n = 23
n=7
n=7 n=6
70
n=7

n = 12
60

50
Trophy hunting targeting
large male horn size

40
‘75– ‘79– ‘83– ‘87– ‘91– ‘95– ‘99– ‘03– ‘07– ‘11–
’78 ’82 ’86 ’90 ’94 ’98 ’02 ’06 ’10 ’12
Year (1975–2012)

Figure 3 | Evolutionary changes in bighorn sheep (Ovis canadensis) horn size in response to variable human trophy hunting pressures. a, Box and
kernel density plots of the horn lengths of male 4-year-old sheep from 1975–2012 at Ram Mountain, Alberta, Canada, where 2.26 male rams were sport-
harvested per year from 1973–1995 followed by a rate of only 0.27 rams per year from 1996–2011. Median values are represented by white circles; box
bottoms and tops indicate the lower and upper quartiles, respectively, whiskers approximate 95% confidence intervals of the medians, and kernel density
is shown in blue. Data are reproduced with permission from ref. 65, Wiley; see the original article for more comprehensive analyses, including with data
from sheep of different age classes and estimates of changes in horn length genetic value. b, Ram Mountain bighorns. Photo courtesy of Gabriel Pigeon.

were ~30% smaller than those in earlier layers dated to ~36,000 to been well documented for many non-human species, including as
24,000 yr bp15. Likewise, in the California Channel Islands, owl lim- changes to behaviour, distribution, and abundance2,37,38,82–85.
pets (Lottia gigantea) have experienced ~40% size reductions since Anthropogenic landscape modifications also create contexts of
the onset of human foraging ~10,000 yr bp80. novel selective pressure, providing a substrate for non-human mor-
In each of the above cases, the observed patterns of morpho- phological evolution16,86. An exceptional example comes from a long-
logical change are inconsistent with known patterns of palaeo­ term study of cliff swallows (Petrochelidon pyrrhonota) in Nebraska,
environmental variation, suggesting that the morphological change where roadside nesting behaviour increased in frequency starting in
probably reflects responses to anthropogenic activity. However, the 1980s with expanding bridge and culvert construction87. Overall
because growth is continuous throughout life for many of these population wing length decreased ~2% across a 30-year period,
taxa, confidently distinguishing adaptive morphological evolu- probably because shorter wings aided flight agility and reduced vehi-
tion from by-products of changes in harvest age profiles based on cle collision risk. Birds killed by cars were consistently longer-winged
archaeological midden data is also a challenge79. Still, such analy- than the overall population, and the frequency of road-killed birds
ses are possible for species with clear markers of growth cessation steadily declined despite the increasing proportion of sport-utility
(for example, for skeletal long bones with their epiphyseal fusion) vehicles over the study period87.
or at least of maturation. For example, sizes of both the largest juve- Human-mediated habitat fragmentation may also exert evolu-
niles and the smallest adult conch (Strombus pugilis) shells became tionary pressures on morphological traits—perhaps especially those
dramatically smaller over the past 7,000 years of human harvesting related to dispersal88. For example, increased wing pointedness in
pressure in Carribbean Panama—conch harvested for food today birds facilitates longer-distance mobility in the face of increased
have ~40% less meat than the conch that existed when human pre- habitat isolation89. By studying museum specimens, Desrochers90
dation began81—demonstrating a morphological evolutionary effect found that songbird relative wing pointedness increased by a mag-
rather than only a mortality profile change. nitude of 7–28% over the last century in North American forests
Without the analytical benefits afforded by extensive shell mid- heavily affected by clear-cutting. The same pattern was not observed
den deposits, archaeologists are more challenged to identify evi- for birds in early-successional and intact forests90.
dence of morphological evolution in response to human harvesting Urban environments in particular are hotbeds for behavioural
pressures on terrestrial vertebrates. Still, Stiner 15 reported a 19% specializations and population density increases among non-human
size decrease (based on humeral shaft diameter as a proxy for body taxa, even while other species have been extirpated91. These environ­
size) for spur-thighed tortoises (Testudo  graeca) that cannot be ments are also home to some of the strongest current examples of
explained by patterns of climatic variation across archaeological non-human adaptation in response to human landscape modifica-
layers dated to 200,000–150,000  yr  bp, 100,000–70,000  yr  bp, and tion92. In a recent study, Winchell et al.93 examined 319 adult male
28,000–11,000  yr  bp at Nahal Meged, a Neandertal and modern Puerto Rican crested anole lizards (Anolis  cristatellus) from three
human site in Israel. independent pairs of urban and nearby forested habitat populations.
Average limb lengths for urban lizards were consistently and sig-
Response to landscape modification and urbanization nificantly longer (~2% longer), and urban individuals also had sig-
Anthropogenic burning and clearing, irrigation infrastructure, nificantly greater numbers of subdigital scales (~3% greater), with
horticultural and pastoral disturbance, and structural investment both traits potentially facilitating more efficient locomotion on arti-
have widespread ecological consequences for other organisms shar- ficial surfaces. Results from a subsequent common garden experi-
ing the affected habitats. Direct and indirect effects or responses to ment suggest a genetic, and thus potentially evolutionary, basis for
human landscape modification—both positive and negative—have the phenotypic differences93. House finches in urban Arizona have

NATURE ECOLOGY & EVOLUTION 1, 0065 (2017) | DOI: 10.1038/s41559-016-0065 | www.nature.com/natecolevol 5

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REVIEW ARTICLE NATURE ECOLOGY & EVOLUTION

Human Affected Magnitude Evol. rate

Species Timeframe Ref.
activity phenotype of change (darwins)

Spur–thighed tortoise
~200 kyr–11 kyr bp Humeral shaft diameter –19% 1 15
Testudo graeca

Mediterranean limpet
~36 kyr–9 kyr bp Shell diameter –33% 15 15
Patella caerulea

Conch
7 kyr bp–Present Shell height –40% 72 81
Strombus pugilis

Giant owl limpet

10 kyr–200yr bp Shell length –40% 52 80
Lottia gigantea

Goat’s eye limpet

~120 kyr–1 kyr bp Shell length –20% 2 79
Cymbula oculus

Argenville’s limpet
~120 kyr–1 kyr bp Shell length –21% 2
5 79
Scutellastra longicosta

Cape turban shell

~120 kyr–1 kyr bp Operculum length –29% 3 79
Turbo sarmaticis

Coyote Femur circumference 118

~20 kyr–10 kyr bp –14% 15
Canis latrans Mandibular gracilization 119

Barley +256%
~4 kyr bp–Present Grain weight 238 148
Hordeum vulgare

Maize +4,000%
~9 kyr bp–Present Number of kernels per ear 429 149
Zea mays

Pumpkin +6,500%
~10 kyr bp–Present Fruit diameter 420 150
Cucurbita maxima

Evolutionary change per

Hunting Invertebrate
Magnitude of change (%) million years (darwins)
harvesting

Extinctions Domestication
≥50 25 0 25 ≥50 1 10 100 1,000 10,000+

Figure 4 | Selected archaeological examples of morphological change in response to human behaviour. The presented magnitudes of phenotypic change
represent approximate percentages of difference from earliest measured value. The reported evolutionary rates (in darwins)130 reflect the magnitude of
morphological change (absolute value of the difference between the natural log of the starting trait value and the natural log of the ending trait value) per
million years. For cases in which multiple phenotypes were analysed, the magnitude of change depicts the first listed phenotype. Photo credits (from top
to bottom): Gisella G.; Esculapio; Daniel Cavallari; Jerry Kirkhart; Jan Delsing; Jan Delsing; MerlinCharon; Justin Johnsen; Leo Michels; US Department of
Agriculture; Arnaud 25.

~2% larger beaks relative to populations in nearby desert habitat, a
putative genetic adaptation to facilitate greater bite forces for con-
sumption of seeds in backyard feeders that are relatively larger and
harder-shelled than those typically processed by the non-urban
finches94. Adaptive beak shape changes associated with feeder-
based diets are also hypothesized for Central European blackcaps
(Sylvia atricapilla)95. However, because bird song acoustics may also
adapt to urban noise environments96 and beak morphology also
modulates song frequency 97, the ultimate evolutionary pressure(s)
affecting urban bird beak shape need to be confirmed.
Response to human-mediated taxonomic turnover
Human population movement, landscape modification, and har-
vesting practices are (and have been) associated with widespread
translocation and extinction of thousands of non-human species.
For example, an incredible number of plant species—more than
13,000, or ~4% of the known extant flora—have been translo-
cated by humans98. While expanding global travel and trade have
led to an increased rate of human-mediated translocation in the
past 150 years99, the purposeful or accidental introduction of non-
domesticated plants and animals to naive ecosystems has a long
prehistory, likely back to the earliest human colonizations of at least
some global landmasses100–102. Invasive species affect endemic taxa
by competitive exclusion, predation, and other processes, com-
pounding the effects of human landscape modification and harvest-
ing pressure to contribute to the ongoing anthropogenic extinction
crisis5,39,99,103,104. In this section we consider the potential effects of
human-mediated turnover in ecosystem species composition on
morphological evolution in non-human plants and animals: either
directly for translocated taxa themselves in response to their new
ecosystems, or indirectly for endemic species affected by invasives
or by the extinction of other species in their ecosystem.
Translocation. Studies of potential morphological adaptation in
translocated species are challenged by the high levels of genetic drift
potentially associated with founder events that may also result in
(non-adaptive) phenotypic change over time105,106, but evolutionary
genomic or fitness analyses may be used to evaluate hypotheses of
neutral versus adaptive evolution in such cases. For example, purple
loosestrife (Lythrum  salicaria), a European wetland plant invasive
to North America, flowers ~20  days earlier and is ~50% smaller
near the northern versus southern extent of its East coast invasive
range107. Based on common garden experiments, these traits are
largely genetically controlled, and strong fitness advantages for ear-
lier reproduction in the north and larger plant size in the south were
identified in transplantation experiments107.
Introduced species can also affect the behavioural ecology
and evolutionary biology of endemic taxa. There is mounting
evidence that prehistoric translocation events induced trophic
cascades with continental-scale impacts on fauna and flora108.
Contemporary examples of the role of invasives in shaping the
morphology of endemic taxa include South American venomous

6 NATURE ECOLOGY & EVOLUTION 1, 0065 (2017) | DOI: 10.1038/s41559-016-0065 | www.nature.com/natecolevol

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NATURE ECOLOGY & EVOLUTION REVIEW ARTICLE
a b
60 n = 4,506

50 n = 351 n = 1,130
n = 55 n = 893
Max operculum length (mm)

n = 396
40

30

20

10

Operculum external surface

0
120 60 12 9 6 3 0
kyr bp
c

Figure 5 | Middle stone age (MSA) to later stone age (LSA) size reductions of Cape turban shell (Turbo sarmaticus) opercula recovered from South
African archaeological refuse dumps (shell middens). a, Box and kernel density plots of opercula maximum lengths from midden layers dating to the
MSA (120–60 kyr bp) and LSA (11–0.5 kyr bp). Median values are represented by white circles; box bottoms and tops indicate the lower and upper
quartiles, respectively, whiskers approximate 95% confidence intervals of the medians, and kernel density is shown in blue. Dotted lines identify the
dated layer boundaries for each sample. Data are reproduced with permission from ref. 79, PNAS. b, Modern Turbo sarmaticus, with operculum external
surface indicated. Photo credit: MerlinCharon. c, Archaeological Turbo sarmaticus opercula that have been micromill sampled for seasonal palaeoclimate
reconstruction, from a Nelson Bay Cave (South Africa) midden layer dated to 9–7 kyr bp. Photo courtesy of Emma Loftus.

fire ants (Solenopsis  invicta), introduced by the 1940s into the
southern United States, where they now prey on endemic fence
lizards (Sceloporus undulatus). Adult fence lizards at sites with the
longest times since ant invasion have 3.4% longer hindlimbs and
have higher rates of body twitching and fleeing responses (which
are more effective in longer-limbed individuals) to fire ant attack
compared with lizards at not-yet-invaded sites109. This pattern
is inconsistent with expected ecogeographic variation based on
morphology of museum specimens collected prior to fire ant inva-
sion, altogether suggesting a recent history of phenotypic adapta-
tion109. Meanwhile, the cane toad was introduced into Australia
in 1935. This invasive species is highly toxic upon consumption
to some but not all endemic snakes, although smaller toads are
less likely to deliver sufficient volumes of toxin to be fatal. Based
on morphological analyses of museum specimens, two snake spe-
cies (Pseudechis  porphyriacus and Dendrelaphis  punctulatus) have
evolved smaller heads over the past 70 years that putatively preclude
the consumption of larger toads110.
Extinction. Human-mediated extinction may have cascading
effects on the evolutionary biology of surviving non-human species
in the same ecosystem, especially when the extinctions involve key-
stone species. We are currently experiencing a mass extinction cri-
sis, with (for example) 8–100 times higher extinction rates over the
past century for vertebrates than the long-term background rate5.
This crisis may be connected to longer-term extinction processes
related to longstanding human landscape modification practices
and harvesting pressures.
Like humans, megafauna are generally keystone trophic facili-
tators for other species in the same habitats111. Of ~150 terrestrial
mammalian genera >44 kg living on Earth’s continents 50,000 yr bp,
approximately 65% were extinct by 10,000 yr bp112. Recent analyses
of new, high-resolution palaeoenvironmental and chronological
datasets have given some (but not all) scholars increasing con-
fidence that colonizing humans played at least indirect roles (for
example, via landscape burning) in prehistoric megafaunal extinc-
tions in multiple large island habitats1,113,114. At continental scales
the role of humans in this process remains less clear 115,116, with natu-
ral climate change likely a major factor in at least certain cases117.
Our purpose is not to draw conclusions from these ongoing inves-
tigations or to review the associated debate. Rather, we suggest that
if our ancestors did play roles in the extinctions of megafauna, then
those events would represent another mechanism through which
human behaviour may have indirectly affected the evolutionary
biology of other (non-megafaunal) non-human taxa. Regardless,
by considering the outcomes of these past events we can raise our
awareness of ongoing and future evolutionary responses to modern
extinction processes.

NATURE ECOLOGY & EVOLUTION 1, 0065 (2017) | DOI: 10.1038/s41559-016-0065 | www.nature.com/natecolevol 7

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REVIEW ARTICLE NATURE ECOLOGY & EVOLUTION

Ecosystem effects from the removal of keystone megafauna likely
included niche space changes and openings for surviving taxa,
resulting in opportunities for morphological evolution that might
be detected in the palaeontological record. For example, in the
~1,000 years following megafaunal extinctions in North America,
coyote (Canis  latrans) femur circumferences—a proxy for body
size—became ~14% smaller relative to those of pre-megafaunal
extinction coyotes118. The observed direction of phenotypic change
is counter to expectations based on contemporary climate varia-
tion, suggesting to the authors that the coyote body size change may
reflect adaptation to a smaller prey base, smaller competitors, or
both118. Furthermore, compared to earlier coyotes, the mandibles
of coyotes in post-megafaunal extinction North America were rela-
tively less robust, and their dental morphology tended more toward
tooth cusp morphology commonly associated with grinding and
omnivory rather than shearing and carnivory 119. These changes are
consistent with morphological evolution in response to megafaunal
extinction-associated dietary shifts.
The vegetation consumption and trampling activities of herbivo-
rous megafauna helped to maintain rich, mosaic-like landscapes;
following megafaunal extinction these structured habitats were
then replaced by denser and less-diverse landscapes111,120,121. Similar
to the above-discussed evolutionary ecology implications of direct
human landscape modification, such changes probably affected
the abundance, behaviour, and perhaps evolutionary biology of
surviving species.
Megafauna also had co-evolutionary relationships with many
large-seeded plants, acting as primary dispersers122. Larger seeds
have higher seedling survival rates123, which probably helps to
explain the co-evolutionary optimization of seed size with dis-
persers. Following extinction of their primary dispersers, some
megafauna-adapted plants still benefitted from secondary dis-
persers124–126, while others without extant dispersers127 have expe-
rienced significant range contractions and even extinction in the
wild128. We predict greater magnitude evolution in fruit and seed
phenotypes facilitating secondary dispersal for the megafaunal-
adapted plants that have best survived this transition. Once in
place, such morphological changes could have aided fruit acces-
sibility for additional dispersers, likewise potentially affecting their
evolutionary ecologies.
In fact, a major component of this process in action has been
documented in Brazil, where larger, seed-dispersing birds (for exam-
ple, toucans, Ramphastos  dicolorus) have been locally extirpated
over the past two centuries from many but not all forest fragments.
Defaunation status accounted for ~34% of variance in seed size; the
proportion of Euterpe edulis palm seeds with diameter > 12 mm (the
size limit for smaller birds) was ~32% in forests with larger birds but
near 0% in defaunated sites129, providing a mechanism for directional
selection on seed size.
are driving morphological evolution in non-human taxa, perhaps
as by-products of rapid human global population growth and
commensurate industrialization. We do not believe that smaller-­
magnitude morphological changes are not also occurring in the
present day—on the contrary, there are likely many, many ongoing
processes that are more subtle and simply below the detection reso-
lution of modern evolutionary biology studies. In contrast, from the
archaeological record we would expect considerable power to detect
non-human evolutionary responses to human behaviour for slower
but longer-lasting phenotypic responses to relatively less-intensive
human activities compared with the examples from modern biol-
ogy 81. Although it is possible that faster rates of evolutionary change
may be less visible in lower resolution (incomplete) archaeologi-
cal records, a temporal increase in the intensity of relevant human
impacts on the environment is the most likely explanation for
the observed difference in the highest observed rates between the
two datasets.
Looking forward, the intensity of anthropogenic impacts on the
evolutionary biology of non-human species will likely continue to
increase, including via additional types of human behaviours and
impact. For example, we have entered a controversial era of human-
directed genetic modification of non-human taxa that includes
realized opportunities to effect morphological changes in existing
species131,132 and the potential to resurrect versions of extinct taxa133.
Rapid climate change is also an ongoing consequence of human
behaviour that can affect non-human evolution134,135. To date, mod-
ern biology studies have been challenged to distinguish genetic-
based morphological adaptations in response to human-induced
climate change from environmental-based (plastic) responses136.
Yet based on the global scale of climate change, we predict that an
unprecedented number of non-human species (that are not other-
wise driven to extinction) could eventually exhibit signs of mor-
phological adaptation to this particular form of human-mediated
ecological disturbance.
Conclusion
Humans are keystone species; our pervasive habitat-modifying and
subsistence behaviours have widespread ecosystem effects, including
on the evolutionary biology of non-human species. Not restricted
to the present, the keystone status of humans and the substantial
ecological impacts of human behaviour extends at least 50,000 years
into prehistory, with associated long-term implications for the evo-
lutionary biology of many non-human taxa. Archaeological and
palaeontological studies that identify non-human morphological
evolutionary responses to past human behaviour—the interpreta-
tion of which can be informed by studies of these evolutionary pro-
cesses in modern systems and vice versa—are thus helping us to
more comprehensively reconstruct the history and significance of
anthropogenic impacts on worldwide ecosystems.

Connecting past, present, and future
To explicitly compare the modern biology and archaeological
observations of non-human morphological evolution in response
to human behaviour we computed the ‘darwin’ statistic as an esti-
mate of the rate of evolutionary change130 for each suitable exam-
ple depicted in Figures 2 and 4. darwins reflect the magnitude of
morphological change per million years. Overall, the observed rates
of morphological evolution in natural (non-domestic taxa) modern
systems are substantially higher than those from the archaeologi-
cal record. Strikingly, present-day human behaviour can apparently
affect morphological evolution in non-human, non-domesticated
species at rates similar to or greater than those associated with
longer-term domestication processes.
The substantially higher evolutionary rates observed in the
modern versus archaeological (non-domestication) records may
reflect recently increased intensities of the human behaviours that
Received 12 September 2016; accepted 20 December 2016;
published 21 February 2017
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Acknowledgements
We thank G. Pigeon, R. Klein and T. Steele for providing the data from their studies
used in Figs 3 and 5; G. Pigeon and E. Loftus for providing images; and M. Aylward,
C. Bergey, R. Bliege Bird, B. Codding, E. Davenport, R. Klein, and D. Schussheim for
helpful comments on earlier drafts of the manuscript. This material is based on work
supported by grants from the National Science Foundation (BCS-1554834 to G.H.P.;
BCS-1459880 to D.W.B.) and by the National Science Foundation Graduate Research
Fellowship Program (DGE1255832 to A.P.S.). Any opinions, findings, and conclusions
or recommendations expressed in this material are those of the authors and do not
necessarily reflect the views of the National Science Foundation.
Author contributions
A.P.S., D.W.B., and G.H.P wrote the paper. A.P.S. and G.H.P. created the figures.
Additional information
Reprints and permissions information is available at www.nature.com/reprints.
Correspondence should be addressed to G.H.P.
How to cite this article: Sullivan, A. P., Bird, D. W. & Perry, G. H. Human behaviour as a
long-term ecological driver of non-human evolution. Nat. Ecol. Evol. 1, 0065 (2017).
Competing interests
The authors declare no competing financial interests.

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