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Biological Journal of the Linnean Society, 2014, 112, 315–331. With 9 figures
Behavioural leads in evolution: evidence from
the fossil record
ADRIAN M. LISTER*
Earth Sciences Department, Natural History Museum, Cromwell Road, London SW7 5BD, UK
Received 10 February 2013; revised 1 August 2013; accepted for publication 1 August 2013
There has been much discussion of the role of behaviour in evolution, especially its potential to lead morphological
evolution by placing the organism in a novel selective environment. Many adaptations of living species can be
imagined to have originated in this way, although documented examples are relatively few. A fruitful arena for
testing hypotheses about behavioural innovation is the fossil record. Traditionally, the behaviour of fossil species
has been deduced from their morphology, precluding the observation of a behavioural lead preceding morphological
evolution. This circularity can be broken by examining behavioural proxies independent of the adaptive morphology
itself. Examples applicable to fossil remains include dietary information (e.g. wear traces on teeth, stable isotopes)
and trace fossils indicating locomotor mode (footprints). The signature of a behavioural lead would be an observed
shift in behaviour from one horizon (or taxon) to another, followed later by a functionally-related morphological
change. This pattern can be sought either in finely-stratified anagenetic sequences of fossils (stratophenetic
approach) or among fossils with well-resolved species-level phylogenies (cladistic approach). An array of case
studies from the literature is presented. These include feeding shifts in finely-resolved sequences of vertebrates
ranging from freshwater fish to terrestrial ungulates, as well as locomotor changes crucial to major evolutionary
transitions in the origin of tetrapods, birds, and humans. The latter examples highlight the role of behaviour in
initiating exaptation (the requisitioning of structure for a new function). The case studies also illustrate the
challenges of using fossil sequences to elucidate behavioural roles, including insufficient stratigraphic resolution
and uncertainty over the adaptive function of observed traits. By the same token, they suggest criteria for choosing
promising cases for research, as well as for formulating testable hypotheses about evolutionary modes. © 2013
The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 315–331.
ADDITIONAL KEYWORDS: Baldwin effect – bird flight – dental microwear – exaptation – footprints –
human bipedality – hypsodonty – stable isotopes – tetrapod locomotion.
INTRODUCTION
There are various processes by which organisms adapt
to their environment (Fig. 1). The core mechanism is
adaptive evolution by natural selection, but adaptation
can also be achieved by phenotypic plasticity, behavioural flexibility, or a shift of range to track a preferred
habitat. There are significant feedbacks among these
processes (Fig. 1). For example, range shifts are
unlikely to leave the population in precisely the same
environment and so natural selection may result.
*E-mail: [email protected]
Phenotypic plasticity may be canalized into a fixed
adaptation by genetic assimilation (Waddington, 1953;
Lande, 2010) or, conversely, natural selection may
favour adaptive flexibility in a highly variable environment, a process that has been termed variability
selection (Potts, 1998). Finally, behavioural accommodation may allow the species to explore a new niche
while the slower process of natural selection adapts
the phenotype accordingly (Hardy, 1965). The latter
process is the focus of the present review.
Behaviour is crucial because it is the means by
which adaptive form is applied to the environment. Although standard accounts of evolution
explain the origin of adaptation by natural selection,
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 315–331
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A. M. LISTER
Figure 1. Modes of adaptive change. A, range (distributional) changes, even when broadly ‘tracking’, place a
population in a new selective regime. B, range reduction
may result in extinction. C, ecophenotypic as well as
genetic change may be adaptive. D, in highly variable
environments, natural selection may favour adaptive phenotypic or behavioural flexibility (‘variability selection’:
Potts, 1998). E, conversely, plasticity may be reduced by
natural selection ‘genetically assimilating’ part of the reaction norm. F, behavioural plasticity may elicit phenotypic
plasticity and vice versa. G, flexible behaviour may lead to
natural selection on behavioural or other phenotypic
traits: labelled the ‘Baldwin effect’ but see text for discussion. H, an organism’s behaviour may modify its own
environment (‘niche construction’: Odling-Smee et al.
2003) and hence its selective context.
they generally sidestep the question of the order in
which a change in form, change in behaviour, and
change in habitat come about. Darwin (1859: 183)
himself stated: ‘It is difficult to tell, and immaterial
for us, whether habits generally change first and
structure afterwards; or whether slight modifications
of structure lead to changed habits; both probably
often change almost simultaneously’ (emphasis
added; see also Fussey & Partridge-Hicks, 2006). He
went on, however, to give examples where ‘habits
have changed without a corresponding change of
structure’, with the clear implication that, given time,
the exploratory population would become physically
adapted to its new niche. Subsequently, various
authors have gone further and suggested that many
key morphological features might never have evolved
had the animal not first explored new habitat and/or
developed new habits (Hardy, 1965; Maynard Smith,
1987). Would the ancestors of the polar bear have
evolved webbed feet before they began swimming in
pursuit of marine prey (Fig. 2)?
Behavioural initiation of evolution includes (but is
not restricted to) aspects of the ‘Baldwin Effect’. This
concept (Baldwin, 1896; Simpson, 1953; Weber &
Depew, 2003) emphasizes phenotypic accommodation
during the lifetime of an organism as a precursor to
longer-term, genetically-based adaptive change (i.e.
evolution). The crucial initiating factor is generally
Figure 2. Could the polar bear have evolved its webbed
feet before it became a marine predator? A, coastal brown
bear with flounder. B, swimming polar bear showing webbed feet. Photo credits: (A) Manuel Presti;
(B) Wikimedia Commons.
seen as behavioural, and this is the focus of the
present review, although many authors (including
Baldwin himself) broadened the concept to encompass
any acquired phenotypic response (Hall, 2003: 147,
table 8.1; West-Eberhard, 2003: 151). A key distinguishing feature of the Baldwin effect is that the
accommodation to the new situation is immediately
‘appropriate’, as opposed to genetic assimilation
where an environmentally-induced trait may or may
not be of adaptive value (Bateson, 2004). It therefore
has more power, in a natural situation, to find the
adaptive ‘needle in a haystack’ on which selection can
act (Maynard Smith, 1987). Bateson (2012) has suggested the term ‘adaptability driver’ to replace the
somewhat inappropriate and confused term ‘Baldwin
effect’.
The behavioural response may be genetically determined, although it can also be the result of cognitive
flexibility (Duckworth, 2009). Flexible behaviour, the
ability cognitively to devise new solutions to problems, is mainly observed in mammals and birds, with
some examples from other vertebrate and invertebrate groups (e.g. cephalopods). Selection can enhance
the tendency to produce the behaviour, especially if it
is persistent (often through learning) within the
population. Additionally, and of particular interest
here, further phenotypic adaptations to the new
niche may evolve. The nature of the behavioural
accommodation is likely to guide the direction of
permanent adaptation (Hardy, 1965); for example, the
dorsoventral flexion of the backbone in the locomotion
of terrestrial mammals ensured the evolution of a
horizontal tail-fluke (rather than vertical as in fishes,
amphibians and aquatic reptiles), whenever they
became secondarily aquatic, in seals, beavers, seacows, and cetaceans.
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 315–331
BEHAVIOURAL LEADS IN THE FOSSIL RECORD
As well as behavioural accommodation to an existing
habitat or resource, dispersal into a new habitat,
selection of microhabitat or modification of habitat (all
aspects of ‘niche construction’: Odling-Smee, Laland &
Feldman, 2003; Odling-Smee et al., 2013) represent
further aspects of behaviour that alter a species’
ecology and may lead to evolutionary change (the
‘eco-evolutionary feedbacks’ of Post & Palkovacs,
2009). By providing ‘ecological inheritance’, niche
construction provides a context of novel selection
pressures that persists across generations, thereby
enhancing the likelihood of adaptive evolution
(Odling-Smee et al., 2013). Recent research has highlighted the importance of intraspecific behavioural
(‘personality’) variation in determining the capacity of
individuals to disperse, and their subsequent success
in founding a population (Chapple, Simmonds & Wong,
2012; Wolf & Weissing, 2012), affecting the likelihood
of subsequent adaptive change and speciation.
Therefore, following Hardy (1965), Bateson (2004)
and others, a broad view of the roles of behaviour in
evolution is taken in the present review. Figure 3
illustrates some alternative scenarios. In the routes
highlighted by filled arrows, behaviour is crucial in
moving the organism into a new environment, and/or
in exploring new niche space with its existing morphology, in both cases leading to adaptive morphological change.
Most literature on behavioural leads in evolution
has been theoretical, sometimes involving modelling
(Hinton & Nowlan, 1987; Ancel, 1999; Zollman &
Smead, 2010; Sznajder, Sabelis & Egas, 2012) but
often essentially discursive (references in Turney,
Bryson & Suzuki, 2008). Thus the plausibility of the
process has been widely discussed, and many existing
adaptations of organisms can be imagined to have
arisen in this way. Demonstrated examples are,
however, relatively few.
Losos, Schoener & Spiller (2004), studying brown
anole lizards, Anolis sagrei, showed that, when introduced to islands with ground predators, the lizards
adapted behaviourally by moving to higher perches
out of reach of predation. This shift led, within 6
months, to significant selection for larger body size
and hindlimb length on islands with predators, interpreted as adaptive to faster escape.
Cubo, Ventura & Casinos (2006) considered the
water vole (Arvicola) complex in Europe, of which
some populations are semi-aquatic and others are
subterranean. Based on a phylogenetic study, they
deduced that the semi-aquatic habit was primitive
and, because only some subterranean populations
show morphological adaptations to digging, they concluded that the unmodified diggers illustrate the
first, behavioural stage in evolution of subterranean
adaptation.
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Sol, Stirling & Lefebvre (2005) found that species of
passerine birds with larger relative brain size (taken
to be a proxy for behavioural flexibility) generally
have more subspecies than those with smaller brains,
and this is not simply a result of greater dispersal
ability. Assuming that subspecies richness implies
local adaptation, the results suggest that behaviourally flexible lineages have undergone greater evolutionary diversification. At a higher taxonomic level,
Nikolakakis, Sol & Lefebvre (2003) found that avian
lineages with larger brains and a higher propensity
for innovative behaviours tend to contain more
species than less flexible lineages.
Badyaev’s (2009) work on the North American
house finch (Carpodacus mexicanus) demonstrates a
remarkable cascade of adaptations in populations
established in different environments, with the high
dispersal ability in this group being considered a key
initiating factor. Yet also for sympatric speciation,
where dispersal is not a factor, likely examples among
insects demonstrate the importance of behavioural
factors such as assortative habitat or mate selection
in initiating the process of divergence (Bolnick &
Fitzpatrick, 2007).
BEHAVIOUR AND EVOLUTION IN THE
FOSSIL RECORD
One of the key advantages of the fossil record is that
it provides, in principle, the possibility of directly
observing evolutionary processes in time series.
Modes of evolution have been studied successfully in
cases where the record is particularly good: generally,
finely-stratified sequences with abundant remains of
the target species in successive layers, allowing a
statistical appraisal of change in morphological traits.
A major avenue of research has been in the adaptive function of such traits, and these, in turn, have
been used to deduce behaviour of the species concerned, and sometimes the palaeoenvironments in
which they lived. Morphological features of marine
fossils, for example, often by analogy with living
forms, differentiate a nektonic or benthic habitat.
Among land vertebrates, limb proportions of extinct
forms suggest their locomotory mode, whereas dental
morphology provides clues to dietary category. Combining several species’ adaptations, the spectrum of
adaptive types across a fossil community has been
successfully used to reconstruct its former environment. Considering locomotory adaptations, for
example, a preponderance of arboreally-adapted
mammals indicates forest, whereas species adapted to
running on open, flat ground would imply a largely
treeless plain (Kappelman et al., 1997). Turning to
feeding adaptations, herbivorous mammals with
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 315–331
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A. M. LISTER
E1/G1/M1/B1
Environment
unchanged
E1/G1/M1/B1
Environment
changes
Alter own
environment
E2/G1/M1/B1
Niche
construction
E2/G1/M1/B1
Move to new
environment
by dispersal
or exploration
E2/G1/M1/B1
Exaptation
E2/G1/M1/B2
behavioural
plasticity
Red
Queen
Extinct
Extinct
Behaviourally flexible
Individuals survive
E2/G1/M1&2/B1&2
E1/G1/M1&3/B1&3
phenotypic
plasticity
Selection of
genetic variants
Assimilation of
ecophenotypic
variants
Better-adapted
ecophenotypic
variants survive
E2/G2/M2/B2
E1/G3/M3/B3
E2/G1&2/M1&2/B1&2
E1/G1&3/M1&3/B1&3
E2/G1/M1/B2
Behavioural solution
inhibits phenotypic
evolution
genetic
variants
Better-adapted genetic
variants survive
E2/G2/M2/B2
E1/G3/M3/B3
Genetic assimilation
of favoured phenotype
Natural selection
of favoured phenotype
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 315–331
BEHAVIOURAL LEADS IN THE FOSSIL RECORD
319
Figure 3. Alternative pathways to achieving new form and function. The example is a hypothetical mammal adapting
to a change from woodland browsing (round snout adaptive, pointed snout even more so) to grassland grazing (flat snout
adaptive). At the circular junctions, any input can lead to any output. Pathways marked by solid arrows are the focus of
the present study, and key potential contributions of behaviour are underlined. E, Environment; G, Genotype; M,
Morphology; B, Behaviour; each can change from an initial state (1) to an altered state (2 or 3). Notes: ‘Niche construction’
may entail either moving to a new environment or altering one’s environment. The ‘extinct’ pathways imply that, without
immediate behavioural accommodation, natural selection or genetic accommodation may not be able to act fast enough
to ensure survival. ‘Exaptation’ occurs when coping in a new environment because existing phenotype is being used in
a new way (although natural selection can also exapt without behavioural help). ‘Red Queen’ evolution (Van Valen, 1973)
implies evolutionary change in an unchanged environment and niche.
◀
high-crowned teeth, flat occlusal surfaces, a low-slung
head, and a wide snout imply grassland, whereas
browsing-adapted species have low-crowned, cuspate
teeth, an elevated head, and narrow snout, and point
to the presence of forest (Eronen et al., 2010).
Although such deductions of habitat and behaviour
from the morphology of species are likely to be
approximately correct for broad units of time and
space, they must logically miss instances where, in an
individual species, behavioural change has preceded
morphological adaptation. Put another way, the
Baldwin effect and related phenomena cannot be
identified on the basis of behaviour deduced from
morphology, because of the inherent circularity of the
logic. To break this circularity, it is necessary to find
indicators of behaviour that are independent of morphology per se. Changes in behaviour and morphology
through time can then be separately traced, and
evidence of behavioural lead sought, as signalled by a
chronological lag between behavioural innovation and
morphological response.
Demonstrated direct proxies for behaviour in the
fossil record include:
• Dental microwear (microscopic scratches and pits
on the occlusal surface of teeth) as evidence of diet.
• Dental mesowear (the shapes into which tooth
cusps wear through use) as evidence of diet.
• Stable isotopes (especially 13C and 15N) preserved in
hard tissues, as evidence of diet.
• Preserved gut contents as evidence of diet.
• Coprolites (fossil dung) as evidence of diet (provided
they can be confidently linked to the culprit species).
• Sub-annual properties (e.g. isotopic composition) of
growth rings in shell, bone or tooth, as evidence of
seasonal migration or dietary variation.
• Abnormal individual growth rings as markers of
stress, or of life-cycle events such as weaning.
• Ontogenetic changes as a result of use (e.g. exaggerated muscle attachments or cortical thickening
of limb bones)
• Other marks on hard tissues as a result of activity
in life (e.g. high incidence of breakage of mammalian carnivore teeth as a result of bone-cracking)
Figure 4. The predicted palaeontological pattern with
(A) synchronous acquisition of new morphology and appropriate behaviour; (B) behavioural lead followed by acquisition of morphology. M1, M2, initial and new morphology;
B1, B2, initial and new behaviour. Solid circle and line,
morphology; dashed circle and line, behaviour. The intermediate phase M1, B2 shows new behaviour but retains
initial morphology (equivalent to the cartoon with the
smiley in Fig. 3).
• Marks on other individuals or species (e.g. toothmarks on prey), provided they can be confidently
linked to the species responsible.
• Preserved trackways as evidence of locomotory
mode (provided they can be confidently linked to
the target species, and bearing in mind that their
form is influenced not only by behaviour, but also
by the morphology of the locomotory organ).
• Aspects of ‘extended phenotype’, such as nests or
hives.
• Rarely, animals preserved ‘in the act’ (e.g. a female
carrying a foetus, or mating insects preserved in
amber).
• Proxy evidence of habitat, from biotic and abiotic
data in enclosing sediment (provided it can be
confidently interpreted as the living, and not just
depositional, environment of the target species).
Other examples of behavioural traces in the fossil
record are described by Boucot (1990) and Boucot &
Poinar (2012).
The standard expectation in palaeontology, of behavioural and morphological change being synchronous,
is illustrated in Figure 4A. If behavioural change preceded the shift in morphology, however, the pattern
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 315–331
320
A. M. LISTER
shown in Figure 4B would be expected. The prediction
is then an initial state with morphology M1 and
behaviour B1; a subsequent stage where morphology is
unchanged at M1 but behaviour has changed to B2
(similar to the +/– stage of Strömberg, 2006: fig. 3); and
a final stage where morphology has changed, perhaps
gradually over time, to M2. That an observed morphological change has occurred in response to a particular
evidenced behavioural change is inevitably a matter of
interpretation; for example, the development of flippers following the move from a terrestrial to an aquatic
habitat can reasonably be interpreted as an adaptation
to swimming. Issues of taxonomy also affect palaeontological interpretation: the studied fossil sequence
might reflect anagenetic change in a single species or
even population, or a sequence of species or populations of demonstrable close relationship but not
necessarily a direct ancestor–descendent series.
Whereas some of the examples presented below are
stratophenetic (dependent on reliable relative ordering
of strata, and with later populations assumed to be
descended from earlier ones), other cases depend on a
cladistic approach, with behavioural proxies treated as
‘characters’ mapped onto the cladogram to estimate
their order of acquisition relative to morphological
features.
Very few palaeontological studies have been undertaken with the explicit intention of testing for a
behavioural role in morphological evolution: these
include those of Miocene sticklebacks by Purnell
et al. (2007), Miocene–Pleistocene ungulates by
Strömberg (2006), and proboscideans by Lister (2013).
However, a review of the literature reveals further
published studies where appropriate behavioural and
morphological data are available. In some of these
cases the authors noted a chronological ‘offset’ between
behavioural proxies and morphological change. A selection of these case studies is reviewed below. They range
from microevolutionary examples with extensive
material and detailed stratigraphic control, to major
innovations in vertebrate evolution where evidence is
more patchy but sufficient to frame hypotheses about
the behavioural role and suggest avenues of future
research.
EXAMPLES FROM THE FOSSIL RECORD
FEEDING ECOLOGY AND BODY ARMOUR IN
MIOCENE STICKLEBACKS
Bell, Travis & Blouw (2006) and Purnell et al. (2007)
studied changes in body armour (bony spines and
plates) in stickleback (Gasterosteus) fossils spanning
20 kyr of a varved (annually-stratified) sequence
from the Miocene of Nevada (Fig. 5). The same
studies also examined feeding ecology using dental
microwear, grounded in studies of laboratory and
wild populations of modern Gasterosteus that
showed clear correlation of microwear score with
benthic versus planktonic feeding habit. In the fossil
samples, feeding habit, deduced from microwear, was
significantly correlated to body armour, with more
benthic-feeding samples showing greater armour
development. At one point in the sequence, a substantial increase in body armour took place within 150
years. This was associated with a shift from planktonic to benthic ecology but, interestingly, the
anatomical changes started 100 years after the
Figure 5. Dental microwear and body armour in sticklebacks. Scanning electron microscope image of (A) tooth of
laboratory planktivorous fish (reproduced with permission; Purnell et al., 2007) showing lower feature density but greater
length of individual features than (B) tooth of laboratory benthic fish; lines mark microwear features (image kindly
provided by M. Purnell). C, heavily armoured Miocene individual with three dorsal spines (D1–D3), seven predorsal
pterygiophores (R1–R7), and a fully expressed pelvis (P) (reproduced with the permission of the Palaeontological Society;
Bell et al., 2006). Diagrams below the specimen indicate the range of pelvic phenotypes and their scores, from 1 (typical
of planktonic populations) to 3 (typical of benthic populations).
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BEHAVIOURAL LEADS IN THE FOSSIL RECORD
habitat change was complete and themselves took a
further 150 years to complete. Purnell et al. (2007:
1887) comment: ‘This evidence of an ecological shift
preceding phenotypic change suggests that this part
of the sequence may record rapid evolution driven by
shifts in trophic ecology and adaptation to benthic
niches’. Caution is expressed that population replacement cannot be ruled out, although the existence of
intermediate phenotypes of all three armour characters scored, in the period of transition (Bell et al.,
2006: fig. 2), argues in favour of an in situ evolutionary transition. The likely selective force for the development of body armour in a benthic habitat is
predation. Moreover, studies of modern sticklebacks
demonstrate that a transformation of this rapidity is
plausible; a newly-colonizing lake population showed
significant phenotypic change within only 20 years
(Aguirre & Bell, 2012), while developmental research
indicates that substantial increase or reduction in
pelvic armour can be achieved through mutation of a
single control gene (Chan et al., 2010).
DIET
AND HYPSODONTY IN
QUATERNARY
TERTIARY
TO
UNGULATES
Many lineages of herbivorous mammals show modification of feeding adaptation in response to the spread
of grasslands through the Tertiary and Quaternary, a
trend in turn resulting from global cooling and aridification. The key dental adaptation, evolved in parallel
in many taxa, was an increase in the crown height
(hypsodonty) of the cheek teeth, generally interpreted
as an adaptation to a more abrasive diet dominated by
grasses, compared to the less abrasive browsing of
broad-leaved plants by their ancestors. Although the
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broad pattern of adaptive change in several groups of
mammals (horses, proboscideans, various artiodactyl
groups) broadly correlates with environmental change,
detailed studies of individual species and genera,
comparing morphological change with dietary proxies
such as stable isotopes and dental wear, are increasingly demonstrating a more complex picture.
African proboscideans
Lister (2013) collated data from various lineages of
Proboscidea (elephants and their relatives) through
the Miocene to Quaternary (approximately 20–0 Mya)
of East Africa, using fossils from radiometricallydated sites. Independent proxies were plotted for
(1) vegetational change, based on δ13C in palaeosol
carbonate; (2) diet, based on δ13C in tooth enamel; and
(3) morphological adaptation, based on molar enamel
ridge count and hypsodonty index. These data show
that, with the beginning of the spread of C4 grasses
at 10–8 Mya (Fig. 6A), various lineages of late
gomphotheres, stegodonts, and early elephants
switched to a diet containing a substantial proportion
of grass, compared to the browsing habit of their
ancestors (Fig. 6B). However, the major adaptive
response, an increase in hypsodonty, is seen only
in later representatives of the elephant lineages
Elephas, Palaeoloxodon and Loxodonta, with only
minor advances until 5 Mya, after which they show
strong directional evolution for more than 3 Myr
(Fig. 6C). This pattern is suggestive of an initial
behavioural shift to grazing, leading eventually to
morphological adaptation.
The ‘lag’ of several million years is remarkable,
however, both in terms of long-term survival with
apparently ‘suboptimal’ dentition and the length of
Figure 6. Evolution of hypsodonty in East African Neogene to Quaternary proboscideans (reproduced with permission;
Lister, 2013, where details of taxa can be found). A, palaeosol δ13C (proxy for vegetation; for sources and site symbols,
see Lister, 2013). B, tooth enamel δ13C (proxy for diet). C, hypsodonty index in upper third molar. In (B) and (C), triangles,
stegodonts and ‘gomphotheres’; circles, elephants; diamonds: tetralophodont/elephantid intermediate. Horizontal lines
mark the interval 8–5 Mya when diet changed (B) but with little morphological response (C).
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A. M. LISTER
time required for morphological adaptation to evolve.
There are several possible explanations for the delay.
First, the major increase in tooth crown height (by a
factor of three in some lineages) required significant
reorganization of cranial morphology and musculature
(Maglio, 1973), which may have taken several million
years to achieve. Second, there may have been other,
more immediate, morphological adaptations that
allowed the initial shift to grazing. The gomphotheres
and early elephants that took up grazing after 10 Mya
do have a slightly increased number of enamel ridges
in their molars compared to their browsing predecessors, an adaptation to grass-eating that temporarily
mitigated the pressure for hypsodonty increase (Lister,
2013). Third, it is possible that the hypsodonty
increase was not an adaptation to grass-eating per se
but, instead, to a later environmental change. The
palaeosol data (Ségalen, Lee-Thorp & Cerling, 2007;
Levin et al., 2011; Cerling et al., 2011; Fig. 6A) indicate
that the spread of C4 grasses was progressive,
commencing approximately 10 Mya and accelerating
from 4 Mya, mirroring the hypsodonty trend in the
proboscideans. Conceivably, the progressive opening
and drying of the habitat led to an increase in grit and
dust on plant food, abrading teeth and selecting for
hypsodonty (Mendoza & Palmqvist, 2008; Damuth &
Janis, 2011; Jardine et al., 2012; Lucas et al., 2013). In
this case, the behavioural switch to grazing led to the
development of hypsodonty more indirectly, by placing
the species in a habitat that later imposed an additional selective force.
North American horses
Mihlbachler et al. (2011) examined hypsodonty
increase in 31 taxa of North American equids through
60 Myr of the Tertiary and Quaternary, with dental
mesowear as the independent dietary proxy (Fig. 7). A
shift to a more grazing habit (probably of C3
grasses) commenced approximately 22 Mya in the
‘Anchitheriinae’ stem-group, coincident with the earliest documented spread of grass-dominated habitats
(Strömberg, 2006), but with only minor changes in
Figure 7. Diet and hypsodonty in North American fossil equids. (A–C) molars showing (A) low crown with browsing
mesowear; (B) intermediate crown with mixed-feeding mesowear; (C) hypsodont crown with grazing mesowear (Hulbert,
2004; reproduced with permission of B. MacFadden); (D) mesowear scores (data points, shaded envelope and white
trendline) and mean molar hypsodonty indices (grey trendline) for North American equids arranged temporally
(reproduced with permission; Mihlbachler et al., 2011). Note offset between white (diet) and grey (morphology) trends,
especially the 16 Myr ‘lag’ between 34–18 Mya. Arrowed points are anchitheriine molars combining mixed-feeding
mesowear with low crown height, and thus are hypothesized to have been under the most intense selection for hypsodonty
increase.
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BEHAVIOURAL LEADS IN THE FOSSIL RECORD
hypsodonty (Damuth & Janis, 2011). The major
increase began approximately 18 Mya with the
advent of the Equini and continued, in tandem
with progressive increase in grazing, for a further
12 Myr (Fig. 7C). Mihlbachler et al. (2011) identify
‘Anchitheriine’ species (in the genera Kalobatippus
and Parahippus, the latter believed to have given rise
to the Equini) with low (browsing-adapted) molar
crowns but mixed-feeding to grazing mesowear, suggesting that these ‘populations pioneering new habitats’ were ‘under the most intense selection for
increased crown height’ (Mihlbachler et al., 2011:
1179, 1181). The authors comment: ‘These observations are consistent with a hypothesis of adaptation
in which the selective regime precedes the morphological change’ (Mihlbachler et al., 2011: 1180). It
may be significant that, among the anchitheres,
Parahippus stands out as having a large number of
individuals with particularly worn teeth (C. Janis,
pers. comm.). Strömberg (2006) suggests that the lag
of 4 Myr between grazing and hypsodonty increase in
horses may indicate that the evolutionary rate was
constrained by the complexity of the required changes
in the whole adaptive complex, including cranial morphology and enamel microstructure, as well as digestive anatomy and physiology.
However, as with the African proboscideans discussed above, it is possible that grass-eating did not
by itself impose selection pressure, and began in a
partially-closed habitat with relatively little airborne
dust to select for hypsodonty, or by grazing tall grass
with relatively little adhering soil. As extensive areas
of grassland opened in North America after 22 Mya
(Strömberg, 2006), a behavioural shift into more open
habitat, and/or a switch to shorter grasses, would
have elicited the selective regime. However, any
interpretation is limited by a lack of direct proxies for
the dust or grit levels experienced by feeding ungulates. Strömberg (2006) cites studies of dental
microwear and the sedimentary context of fossil
horses suggesting little evidence of significant grit
ingestion during critical phases of horse evolution
and therefore considers adaptive lag a more plausible
explanation.
Other examples
Studies of several other groups of fossil mammals also
indicate an apparent discrepancy between feeding
and morphology (Mihlbachler & Solounias, 2006;
Strömberg, 2011; Jardine et al., 2012), even if there
are not always sufficient data to examine chronological trends. Three examples are given below.
In a study of the extinct North American ruminant
group Dromomerycidae, Semprebon, Janis &
Solounias (2004) found that, in general, adaptive
morphology correlated well with diet indicated by
323
microwear and mesowear, but in some cases did not.
For example, species of the Late Miocene Cranioceras
show tooth-wear indicative of mixed-feeding (i.e.
incorporating grass as well as browse) but retain a
skull morphology similar to ancestral browsing
species.
The
authors
suggest
that
‘some
dromomerycid taxa might have been eating food
materials that they were not optimally adapted to
handle efficiently’, and that ‘skull morphological
changes may lag behind actual dietary practices’
(Semprebon et al., 2004: 438, 440). In the contemporaneous and closely-related Pediomeryx, a similar
mixed-feeding profile is associated with derived
cranial features more adapted to grazing, suggesting
a second stage in the process. This study is important
in that it considers dietary adaptations other than
molar hypsodonty (cf. Jardine et al., 2012). Although
the evolution of hypsodonty might depend on selection as a result of dietary grit and hence not coincide
with a shift to grass-eating, cranial adaptations (for
example the broader muzzle in grazers than browsers) relate directly to the cropping and chewing of
plants of different types and heights (Mendoza, Janis
& Palmqvist, 2002). They therefore would have been
expected, if their modification were coincident with
behavioural change, to have changed in step with the
proxy evidence of dietary shift.
Studying oreodonts (an extinct group of North
American artiodactyls of uncertain affinity),
Mihlbachler & Solounias (2006) found wide variation
in diet (evidenced by mesowear analysis) through the
Cenozoic, both within and between species, which did
not always correlate to hypsodonty. These include
low-crowned species with periodically significant
grass intake that may have been behaviourally
‘pushing the boundary’, together with derived, relatively hypsodont species assumed to be capable of
eating a variety of plant types and therefore under
relaxed section, illustrating the two stages (if not in
ancestor–descendent relationship) of the process of
adaptation.
MacFadden & Shockey (1997) examined a range of
herbivorous mammals in the Pleistocene of Bolivia,
determining feeding habit (C4 grazing versus C3
browsing) from δ13C in tooth enamel. Most species
showed a correlation between C3 intake and
hypsodonty index but three brachydont species
showed a strong grazing signature. These were the
gomphothere proboscidean Cuvieronius (analogous to
the grazing gomphotheres of the African Late
Miocene; see above) and two camelids: a species of
Llama, and a species comparable to Vicugna. Damuth
& Janis (2011: 751) comment: ‘Were such animals . . .
caught at a moment of time when they were struggling to maintain themselves in the face of an
inappropriate diet?’. This would imply an interval of
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 315–331
324
A. M. LISTER
strong selection rarely caught in the fossil record
(Mihlbachler & Solounias, 2006), even if, in this
example, there is no opportunity to look for an evolutionary response in morphology, since the assemblage is geologically very recent. The alternative
explanation, a lack of selective pressure because of
low dust levels in a semi-closed environment, cannot
be invoked in this instance because palaeobotanical
evidence indicates a very largely open habitat (97%
grass pollen) with only scattered trees and shrubs
(MacFadden & Shockey, 1997).
THE
ORIGIN OF TETRAPOD LOCOMOTION
The origin of terrestrial locomotion in land-living
vertebrates entailed many morphological innovations
in the transition from fins to limbs, including the
development of feet with digits, pelvic apparatus connected to the vertebral column by a sacrum, limbs
able to move in a ‘walking’ fashion, and associated
musculature. Current evidence suggests that the first
limbed vertebrates were primarily aquatic and that
digitated limbs evolved before the ability to walk on
land (Clack, 2009).
King et al. (2011) studied locomotion in the living
Protopterus, a member of the lungfish, the extant
sister-group to the tetrapods. This fish ‘walks’ underwater using its elongated bony fins to propel itself
against the substrate. The predominant use of the
pelvic (hind) fins, the alternating as well as bounding
gaits, and the body held aloft above the substrate, all
recall tetrapod locomotion and may provide one model
for its origin. Although lungfish are not the direct
ancestors of tetrapods, Protopterus is of interest in the
present context in that it shows walking behaviour
preceding ‘any obvious morphological specialisation
for walking’ (King et al., 2011: 21149). It is possible,
therefore, that behaviour of this kind prefigured the
evolution of quadrupedal walking, with or without
digits, and subsequently the origin of digitated feet.
The authors point out that the other extant
sarcopterygian (lobe-finned fish), the coelacanth
Latimeria, also uses an alternating ‘gait’ in its fin
movements (albeit not against the substrate), so this
behaviour may be primitive for the group that
included the ancestors of tetrapods.
In the fossil record, some hints of modification of
forelimb elements toward a support function are
seen in the most derived tetrapodomorph fish
(Panderichthys and Tiktaalik), although the
pattern of origin of the digitated limb remains
essentially unknown (J. Clack, pers. comm.). Recent
biomechanical analysis of the skeleton of the early
tetrapod Ichthyostega (approximately 380 Mya) suggests propulsion by the front limbs pushing side-byside against the substrate, with the hind limbs
Figure 8. Early tetrapod locomotion. A, trackway from
the Devonian of Poland, showing manus and pes prints
in diagonal stride pattern; presumed direction of travel
from bottom to top. B, generic Devonian tetrapod
based on Ichthyostega and Acanthostega, fitted to the
trackway. Reproduced with permission (Niedźwiedzki
et al., 2010).
incapable of walking and probably used as paddles
(Pierce, Clack & Hutchinson, 2012). This mode of
locomotion differs from that observed in the living
sarcopterygians (see above). It may represent an
enhancement of aquatic adaptation in a lineage not
directly ancestral to tetrapods. If primitive for
tetrapods, however, it predicts a complex and currently undocumented behavioural transition to terrestrial walking.
Remarkable, early tetrapod tracks are preserved
in the Late Devonian (approximately 395 Mya) of
Poland (Fig. 8; Niedźwiedzki et al., 2010). These
include isolated impressions of digitated feet that
could have been made by a creature similar to
Ichthyostega or Acanthostega. There are also series of
smaller prints arranged in trackways, implying a
pattern of walking involving all four limbs in alternating strides with the body clear of the substrate,
which are features of terrestrial tetrapods. The
trackway impressions are simple, without impressions of digits, and it is uncertain whether their
maker had a fully-formed foot or not. It is therefore
not yet possible to confirm whether quadrupedal
walking behaviour arose after the acquisition of a
digitated foot, which is implied if the Ichthyostega
model of locomotion is primitive, or before it, as
suggested by the Protopterus study.
THE
ORIGIN OF AVIAN FLIGHT
Extant birds possess a highly-modified complex of
skeletal structures used in flight, as well as
associated soft-tissue features of musculature,
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BEHAVIOURAL LEADS IN THE FOSSIL RECORD
respiratory system, nervous system, and so on. It is
now widely accepted that birds evolved from bipedal
theropod dinosaurs (Chiappe, 2007), and recent years
have seen the discovery of a remarkable array of
feathered dinosaurs and early birds, especially from
China. These finds illustrate the assembly of the
avian body plan through a series of increasingly birdlike transitional anatomical stages. At the same time,
many different models for the origin of flight have
been proposed, from arboreal gliding to terrestrial
jumping or running, including catching prey (Heers &
Dial, 2012: table 1). Strikingly, almost all of these
models are centred on behaviour, proposing that
feathers, proto-wings, and associated structures
evolved initially for functions other than flight but,
through their ability to provide lift, they became
modified in stages for increasingly sophisticated
flight.
Direct evidence of locomotory behaviour is limited
in known fossil theropods and birds. However, juveniles of living birds show transitional skeletal and
feather morphologies that are remarkably similar to
those of extinct theropods, and their locomotor capabilities provide convincing evidence with respect to
form–function relationships in the extinct forms, and
the behavioural stages leading to the development of
true flight. In this way, the well-documented
theropod record can be interpreted to illustrate the
stepwise acquisition of a character complex by successive, alternating innovations in behaviour and
morphology.
Heers & Dial (2012) show how, in living birds such
as the chukar (Alectoris chukar), juveniles lack many
of the flight adaptations of adults, with unfused thoracic vertebrae and sacrum, small pelvis, very small
keel (sternum extension that attaches flight muscles),
and feathers that are symmetric (vanes the same
width on either side of shaft). In all these features,
they are similar to theropods, and as young birds
mature these features develop in partial ‘recapitulation’ of the evolutionary sequence in the fossil record.
Of particular interest are the ways young birds utilize
these morphologies in locomotion. In chukar, 7–8-dayold chicks engage in wing-assisted ‘flap-running’ up
inclines, and controlled flapping descent (e.g. from a
perch), their underdeveloped wings and feathers providing limited but useful aerodynamic force. Older,
18–20-day-old individuals, with more developed
skeleton and feathers, are additionally capable of
brief episodes of flight. Given the similarity of
their anatomy to theropods with proto-wings and
symmetric feathers, and support from biomechanical
reconstructions (Hutchinson & Allen, 2009), these
behaviours appear likely for bird ancestors and would
have provided the selective context in which true
flapping flight could evolve.
THE
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EVOLUTION OF BIPEDALITY IN HOMININS
The origin of habitual bipedality in humans, from a
largely arboreal, quadrupedal ancestor, involved a
suite of anatomical modifications to the skeleton. In
the hind limb, the foot transformed from a grasping
structure to a weight-bearing platform with shorter
toes, a large non-opposable hallux, a large heel, and
an arch. The hip and knee joints enlarged and the
vertebral column was placed closer to the hip joint.
Leg length increased and the femur became slightly
angled medially to form the ‘bicondylar angle’ bringing the knees under the body during walking.
One of the earliest known hominin fossils, Orrorin,
already shows at approximately 6 Mya clear bipedal
adaptations in its hip joint, specifically a spherical
and anteriorly-rotated head and elongated neck of the
femur. Other parts of the skeleton, including curved
phalanges, indicate a retention of tree-climbing adaptation (Richmond & Jungers, 2008). The foot of
Ardipithecus, more than 4 Mya old, similarly has
several features suggestive of bipedalism but retains
ape-like features such as a very divergent big toe. It
was probably both a tree-climber and an occasional
upright walker. Various species of Australopithecus,
in the range 4.0–1.5 Mya, show further modifications
of the foot toward bipedal adaptation, including a
more aligned hallux and the presence of a longitudinal arch, but, overall, their skeletons suggest a facultative ability to both walk and climb trees.
Direct behavioural evidence comes in the form of
preserved footprints, both the shape of the individual
print and the pattern of walking indicated by
trackways. The earliest are from the Laetolil beds,
Tanzania, approximately 3.7 Mya and generally
attributed to Australopithecus afarensis (Fig. 9).
Recent experimental and simulation work (Raichlen
et al., 2010; Crompton et al., 2012) has demonstrated
that the Laetoli hominins walked erect with weight
transfer similar to the economical extended-limb
bipedalism of modern humans. This bipedal functionality was implemented largely by soft-tissue innovation but with an internal bony configuration differing
from that of modern humans; for example, in the less
expanded hallux (big toe) (Crompton et al., 2012).
A further line of evidence on behaviour is provided
by epigenetically sensitive traits that are modified by
an individual’s activity pattern (Ward, 2002). In
Orrorin, for example, cortical bone is thicker on the
lower side of the femoral neck than on the upper side,
in contrast to the situation in great apes but similar
to that in humans. The difference is considered to be
a result of bone remodelling in response to the configuration and usage of the limb abductor muscles in
life, and is interpreted as providing ‘direct evidence
for frequent bipedal posture and locomotion’ in
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326
A. M. LISTER
Figure 9. The origins of human bipedality. A, footprint trail cf. Australopithecus afarensis from Laetoli, Tanzania. B,
false-colour depth maps of (left) Laetoli mean footprint and (right) modern human. Redder shades within the ‘footprints’
indicate greater mean depth. Reproduced with permission (Crompton et al., 2012). C, wild chimpanzee walking bipedally
while carrying three papayas (one in each hand and one in mouth). Reproduced with permission (Carvalho et al., 2012).
Orrorin (Galik et al., 2004: 1453). The bicondylar
angle of the femur is also an epigenetically labile
trait: in a study of normal and non-ambulatory children, the existence of the angle was found to be
the result of a habitual bipedal gait; it does not
form in individuals who engage only in intermittent bipedality (Ward, 2002). Its presence in
Australopithecus is therefore taken to demonstrate
that it was a habitual biped.
Overall, hominins from Orrorin to Homo habilis
show a varying mosaic of ape-like and human-like
locomotory morphology (Harcourt-Smith & Aiello,
2004; Richmond & Jungers, 2008), an essentially
human bony foot first appearing in Homo erectus. A
footprint trail from Ileret, Kenya, at approximately
1.5 Mya, and assigned to Homo ergaster/erectus, is of
modern form, with more longitudinally-aligned hallux
and a narrower instep than the Laetoli prints
(Bennett et al., 2009), and a strong ball and hallux
impression indicating the antero-medial weight transfer that is the hallmark of modern human walking.
The likelihood that the ancestors of H. erectus,
whichever among the array of known species they
were, showed facultative terrestrial and arboreal
behaviour, implies that positive selection was stronger
on the terrestrial mode, leading to anatomical modification to optimize for terrestrial locomotion at the
expense of tree-climbing. Alternatively, it has been
suggested that arboreal behaviour cannot be confidently deduced from the retention of primitive anatomical traits and that A. afarensis and related species
were already obligate bipeds (Harcourt-Smith &
Aiello, 2004). This scenario only strengthens the cardinal importance of their bipedal behaviour in providing the selective context for ‘modernizing’ their
anatomy.
Recent studies of orangutans (Pongo pygmaeus)
and chimpanzees (Pan troglodytes) graphically
illustrate alternative possible first steps towards
bipedality in an essentially arboreal human ancestor.
The two examples occur in very different contexts
but both rely crucially on behavioural innovation,
in species lacking the morphological adaptations
to bipedality discussed above. Modern chimpanzees
adopt temporary bipedality at ground level to carry
objects by hand (Fig. 9C; Carvalho et al., 2012). Orangutan, by contrast, walk bipedally along branches,
while the hands are used for feeding, balance or
weight transfer (Thorpe, Holder & Crompton, 2007).
Evidence that one of these modes was at the origin of
hominin bipedality would be a convincing case of
behavioural flexibility leading morphological evolution. Such evidence might come in the form of early
(> 6 Mya) bipedal trackways made by an essentially
unmodified foot, especially if linked to a species considered to be a potential ancestral hominin.
DISCUSSION
FOSSIL
SAMPLING
The case studies discussed above vary in the degree to
which they meet the ideal requirements for demonstrating behavioural leads in evolution. However, all
fulfil the key requirement of providing at least some
behavioural proxy data independent of adaptive morphology. In one case, the theropod-bird transition,
the model is somewhat stretched because the behavioural evidence for proto-flight comes not from the
fossils themselves but from the behaviour of
morphologically-similar modern analogues.
The second requirement is for an adequate fossil
record, either in the form of a finely-stratified sequence
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BEHAVIOURAL LEADS IN THE FOSSIL RECORD
of ancestor–descendent populations (stratophenetic
approach) or a well-resolved cladogram of closelyrelated taxa (cladistic approach). The varved Miocene
sequence of Nevada (Purnell et al., 2007) is a nearideal system, allowing a lag of only 100 years to be
observed between behavioural and morphological
change in the stickleback fish. In many other areas of
the fossil record, it may be impossible to determine
whether an observed ‘simultaneous’ appearance of new
morphology and matching behaviour reflects genuinely simultaneous acquisition, or a behavioural lead
too short to be observed with the given stratigraphic
resolution. We must also acknowledge that some evolutionary responses, especially where suitable genetic
variation and developmental pathways are already
available, may be essentially synchronous with the
behavioural driver (Post & Palkovacs, 2009), so no ‘lag’
would be detectable even in the most finely-stratified
fossil sequences.
The theropod-bird and horse studies are examples
of successful analysis of behaviour and morphology
based on cladistically-ordered sequences of species.
Other, potentially interesting examples were excluded
from discussion because of incomplete knowledge
of relationships. For example, Miocene beavers
Stenocastor show evidence for swimming behaviour in
their claws but had not evolved a flattened tail
(Hugueney & Escuilllé, 1996). However, Stenocastor
is not considered close to the ancestry of modern
Castor, and current evidence is insufficient to establish whether swimming adaptations evolved once or
more than once in the group.
FUNCTIONAL
INTERPRETATION
Some of the cited examples illustrate evolution in a
character with direct functional relationship to the
observed behaviour (e.g. the evolution of hypsodonty
in mammals switching to more abrasive food). In
other examples, morphology has changed in response
to other aspects of the new niche (e.g. the development of body armour in sticklebacks switching to
feeding in the benthos).
Whether an observed morphological change has
occurred in response to a particular behavioural
change is, however, a matter of interpretation. As
noted by Strömberg (2006), temporal coincidence of
behavioural and morphological change is evidence for
their adaptive link, but the longer the ‘lag’, the harder
it is to apply this criterion. The other main line of
evidence is functional interpretation of the observed
morphology, although this may not be obvious or can
be erroneous. For example, the question of whether
hypsodonty in ungulates is adaptive for grass-eating
per se, or to life in an open environment, is disputed,
as discussed above. Similarly, the cranio-dental
327
morphology of certain australopithecine hominin
species was assumed to be adapted to cracking hard
foods, but this is not substantiated by microwear and
isotopic studies (Grine et al., 2012). Either the morphology in question evolved for a different function, or
else it was not, at the time of sampling, being utilized
for the function for which it was originally selected.
There is also, however, the issue of correct interpretation of the behavioural proxy. Lucas et al. (2013)
provide evidence that scratches in hominin dental
microwear are primarily the result of abrasion by
mineral particles, and may not accurately reflect food
type (e.g. grass-eating) as previously assumed.
Finally, we must recognize that an animal’s potential repertoire of behaviour is not decoupled from its
anatomy: physical structure constrains which behaviours are possible. For example, biomechanical study
of the early tetrapod Ichthyostega (Pierce et al., 2012)
suggests restricted shoulder and hip mobility, so the
animal lacked the necessary rotary motions to push
the body off the ground and move the limbs in an
alternating sequence. The paddle-like hind limb,
moreover, was quite strongly adapted to aquatic locomotion. Quadrupedal walking may not have evolved
from an Ichthyostega-like morphology but, if it did,
initiation of walking would have had to wait for
permissive morphological change. Only once appropriate structures are available, are they capable of being
behaviourally co-opted to new function.
EVOLUTIONARY
PATTERN AND PROCESS
The ideal sequence illustrating a behavioural lead is
the three-stage pattern illustrated in Figure 4, including the crucial transitional phase of unaltered morphology but modified behaviour (M1, B2). The initial
behavioural shift might be seen in all sampled individuals of a species, or only in some individuals or
populations. The latter would be interesting in suggesting behavioural variation, with the more exploratory individuals testing the new niche space. Such
individual variation is seen in Figure 6 (African
proboscideans) and Figure 7 (North American horses).
It is impossible, however, given the incompleteness
of fossil remains, to be certain that no morphological
innovations were providing adaptation during the
transitional interval of apparently purely behavioural
accommodation. This would include soft-tissue or
physiological changes not preserved in the fossil
record, although we can at least search thoroughly for
any change in preserved hard parts. A degree of
anatomical modification during the phase of behavioural innovation does not preclude the essential role
of the behaviour in precipitating further morphological change. An example is seen in the case of African
proboscideans, where minor dental modifications
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A. M. LISTER
accompany the switch to grazing but are later followed by much more profound ones (Lister, 2013). The
new behaviour and niche, albeit with the aid of
already slightly modified anatomy, have elicited
further anatomical specialization.
It is evident that the interplay of behavioural and
morphological change is an ongoing, sequential
process, especially in the building of complex character assemblages such as that associated with flight in
birds: each anatomical modification is likely to be
associated with a shift in behavioural repertoire, creating the context for the next innovation, and so on.
Behaviour leading morphology is, however, not the
only possible pattern of change. Many advantageous
mutations do not require behaviour at all to be positively selected; for example, the first mutant theropod
with proto-feathers could have been selectively
favoured thanks to enhanced thermoregulation. Only
later might behaviour have been involved in exapting
the feathers for flight. In another model, mutation
affecting morphology might lead the animal to adopt
novel behaviours to survive, which, if successful,
could result in selective spread of the new phenotype:
the inverse to the ‘behavioural lead’ model. A celebrated example is the goat born without front legs
that learnt to walk bipedally (West-Eberhard, 2003:
51). Dover’s (2000) concept of ‘adoptation’ postulated
genetic processes leading to anatomical change,
organisms then seeking out an appropriate habitat or
niche. Finally, theory has suggested that behaviour
may in some circumstances inhibit morphological
adaptation (Duckworth, 2009). Provided independent
behavioural proxies and an adequate fossil record are
available, it is in principle possible to test between
these various modes, or at least between their predictions regarding the temporal relationship of behavioural and morphological change.
A further potentially important factor is the role of
phenotypically plastic morphology, if an adaptive
region of the reaction norm becomes fixed by selective
narrowing of the developmental spectrum (Fig. 1:
genetic assimilation). Phenotypic plasticity (Lande,
2010; Piersma & van Gils, 2010) complicates the
tracing of the behaviour–morphology interaction in
the fossil record, in that observed morphological
change might be part of a pre-existing reaction norm
rather than adaptively selected during the timeperiod under study. It is not always possible to determine from the fossil record whether an observed
morphological change is genetically-determined (i.e.
an evolutionary change) or an expression of phenotypic plasticity (ecophenotypic change). The latter is
often limited to relatively simple changes in body size
or form, and is more readily reversible (Lister &
Green, in press); even so, more complex, long-term
phenotypic changes could be initiated, at least,
ecophenotypically (Pfennig et al., 2010). However, this
is a general issue in the interpretation of adaptive
morphology in the fossil record, and is not limited to
the study of behavioural leads. An ecophenotypically
altered morphology could itself also interact with
behavioural innovation in leading to fixed phenotypic
change.
External factors influencing the process (the
‘change of environment’; Fig. 1) include not only
physical factors such as climate and topology, but also
other animal or plant species in a competitive, synergistic, predatory or prey relationship to the species
under consideration. Competition, for example, is a
likely driver of the original behavioural shift in many
cases, and may subsequently select for character displacement (Pfennig & Pfennig, 2012). The external
environment can also be altered by behaviour, not
only at the level of the individual organism (niche
construction) but, also, in larger-scale ‘ecosystem
engineering’, such as burrowing and bioturbation,
affecting many species as well as those responsible for
the initial behaviour (Erwin, 2008).
A key conclusion of this review is recognition of the
potential importance of behaviour in the process of
exaptation (cf. Strömberg, 2006). Behaviour can forge
a new use for a structure provided it has some functionality in that role (i.e. it is ‘preadapted’) and can
become exapted by further modification. Thus, the
proto-wings of theropods, if originally evolved for
functions other than flight, could have provided lift
when flapped in an appropriate fashion. Similarly, the
tetrapod hind-foot, if it initially evolved for swimming
(as in Ichthyostega), may later have been exapted for
terrestrial locomotion. Behavioural exaptation to a
new role can be predicted almost always to lead to
evolutionary structural refinement.
The behaviour of an organism is often more proximal to selection pressure than the structure itself,
constituting the activities that allow the individual to
survive and reproduce. Selection on behaviour will
‘drag’ with it the morphology, or any other aspect of
phenotype, that is utilized in, or facilitates, the
behaviour. For example, it was suggested above that
preferential selection for terrestrial behaviour in
hominins, from an ancestor with a dual, facultative
terrestrial and arboreal habit, led to terrestrialization
of the locomotory apparatus.
We must be careful not to regard a lineage as
‘heading’ to a supposed optimal condition seen today
or in its terminal members. If the behaviour and
morphology of a fossil species were in the process of
adapting, it was toward evolutionary equilibrium
with its environment at the time. Nonetheless, the
adaptive process, especially the evolution of complex
structure, must take time, implying that species are
not always optimally adapted to a rapidly changing
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BEHAVIOURAL LEADS IN THE FOSSIL RECORD
environment. Nor is it teleological to regard the
modern human foot as more optimally adapted to
bipedal walking (e.g. in mechanical or energetic
terms) than that of our ancestors who first took up
bipedality.
FORWARD
VIEW
This brief review illustrates the potential of the fossil
record, with its chronological perspective over different time-scales, and available behavioural proxies as
well as hard-tissue morphology, to illustrate the role
of behaviour in phenotypic evolution.
Together with controlled present-day experiments
such as those of Losos et al. (2004), palaeontology can
lead us, beyond mere plausibility arguments, to concrete examples. Accordingly, we need to treat trace
fossils as evidence of the behavioural factor in evolution rather than merely as proxies for morphology.
This will allow us to progress beyond the common
palaeontological assumption of a lock-step between
morphology and behaviour and, instead, explore the
chronological relationship between them and test
hypotheses of process. The length of time that morphology takes to evolve, following a behavioural innovation, is one important question, both in terms of
survival capacity during the ‘lag’ period, and the rate
of construction of new adaptations. Another is the
likely life-history consequences of a period of ‘suboptimal’ adaptation; for example, switching to abrasive food with low-crowned teeth is likely to reduce
life-span and select for rapid reproduction and,
perhaps, reduced body size.
The behavioural model can also lead to specific,
testable predictions in particular cases. For example,
occasional bipedality in chimpanzees, as a model
for the first stages in human upright walking,
would predict bipedal trackways made by a hominin
ancestor with still-unmodified ape-like postcranial
morphology.
As the above discussion makes clear, only in some
cases are fossil data sufficient to allow the behavioural role in evolution to be teased from its morphological consequences. By the same token, however, we
can move proactively to hypothesis-testing by seeking
and selecting case studies where data fulfil the necessary requirements.
ACKNOWLEDGEMENTS
I am most grateful to Jenny Clack, Paul Barrett,
Isabelle de Groote and Robin Crompton who kindly
read parts of the manuscript and provided invaluable
suggestions. I am also very grateful to Christine
Janis, John Odling-Smee and Mark Purnell for their
insightful comments that significantly improved the
329
final paper. Finally, I thank Richard Hulbert and
Bruce MacFadden for help with acquiring published
images.
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