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Adaptation

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DOI: 10.1007/978-94-017-9014-7_5

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Chapter 5
Adaptation

Philippe Grandcolas

Abstract Adaptation is a concept central to evolutionary biology that explains why

organisms fit their environment according to natural selection. An adaptation can be
defined as a novel character appearing in an organism and maintained by natural
selection. This concept must therefore be studied at two different levels, within a
phylogenetic analysis for inferring relative novelty and within a populational analy-
sis to assess the role of natural selection. By addition of these two study levels, ad
hoc or tautological proposals of adaptive characters may be avoided. The related
concepts of preadaptation or exaptation feature the importance of considering both
a structure and its function to better understand the evolution of a character. The
structure can remain stable and the function can change, subsequently contributing
to an evolutionary innovation.

Living organisms inherit their characteristics by descent with modification. This

general and basic process assumption explains the diverse range of situations
observed with regard to biological evolution. Therefore, biological diversity is
inferred to result from species divergence after successive modifications that
occurred during the course of evolution. If the process of descent with modification
explains the diversity of organisms well, it does not, however, explain the fit of
organisms to their life conditions. Why species divergence does not occur by diver-
sification in every phenotypic direction and why it often produces a better fit of
species to their environment. For example, why a species of insect that shelters on
trees shows the detailed aspect of a leaf not only to our eye but also to that of the
predator. Why the different biological parameters involved in life histories and pop-
ulation dynamics are arithmetically adjusted to each other? To explain all these fits,
one assumption more than descent with modification must be included in the pro-
cess assumption, the one about the particular case of adaptation. Adaptations are
inherited modifications of organisms, which are not maintained stochastically or
independently of the environmental influence. These modifications that we know to

P. Grandcolas (*)
UMR 7205 CNRS, Institut de Systématique, Evolution et Biodiversité,
Muséum National d’Histoire Naturelle, 45, rue Buffon, 75005 Paris, France
e-mail: [email protected]; http://isyeb.mnhn.fr/

© Springer Science+Business Media Dordrecht 2015 77

T. Heams et al. (eds.), Handbook of Evolutionary Thinking in the Sciences,
DOI 10.1007/978-94-017-9014-7_5
78 P. Grandcolas

be heritable have been assumed to be maintained by natural selection since Darwin

(1859). Darwin and Wallace established the theory of natural selection in a scientific
context where the notion of biological evolution itself was largely recognised (cf.
Perrier 1886; Mathews 1958). Since that time, scientists have searched for an under-
standing of the role of natural selection in the construction and maintenance of
extremely diverse adaptations. These research projects have often been very suc-
cessful but they have also led to some exaggerations or ad hoc explanations fol-
lowed by controversies. The succession of achievements and controversies during
150 years has sometimes cast doubts on the heuristic value of the adaptation con-
cept. Some biologists were afraid that this concept could be detrimental to the whole
theory of evolution, by favouring narrative and inductivist over hypothesis-testing
approaches. However, to explain the fit of organisms, the concept of adaptation
remained unavoidable and it was to Darwin’s (1859) great merit that he understood
it and carefully exposed it.

1 The Concept, Its Definition and Its Implications

An adaptation can be defined as a novel character appearing in an organism and

maintained by natural selection.1 There are many subtle and somewhat confused
variants of this definition, each of them linked to different uses in varied scientific
domains.2 In the present definition, the adaptation is the character itself but the term
is also used to name the process by which this so-called adaptive character has been
acquired by the organism. In all cases, this definition clearly refers to two important
aspects of the concept of adaptation.
Adaptation should be worked out at two different observation levels. The
first level allows one to detect if the character is an evolutionary novelty (a new
character appeared in an organism and was maintained by natural selection),
by the way of phylogenetic analysis relating species according to their shared
original characters, the apomorphies.3 By definition, an apomorphic character,
original and shared by several species, is an evolutionary novelty, and therefore
only a possible adaptation of these species. Conversely, every adaptation of one
or several species is, by definition, a novelty at this level, thus an apomorphy.4
To detect an evolutionary novelty and therefore to bring the first corroboration
for the occurrence of an adaptation, a phylogenetic analysis must be carried out
to check if the putative adaptation is actually an apomorphy of the taxon con-
sidered (Fig. 5.1). The second level of observation deals with the role of natural
selection (a new character appeared in an organism and was maintained by nat-

1
Antonovics (1987), Coddington (1988), Brooks and McLennan (1991), Leroi et al. (1994),
Grandcolas and D’Haese (2003).
2
For example, Sober (1984), Rose and Lauder (1996), Mahner and Bunge (1997).
3
See Hennig (1965, 1966), Wiley (1981), Farris (1983).
4
See Coddington (1988), Grandcolas et al. (1994), Deleporte (2002), Grandcolas and D’Haese (2003).
5 Adaptation 79

Fig. 5.1 An adaptation is, by

definition, an evolutionary
novelty. In this simple
theoretical example, the three
more nested taxa acquired
the trait “A” with the function
“1.” From the phylogenetic
point of view, the trait
“A” can be an adaptation

ural selection). This role can only be studied with respect to processes of dif-
ferential survival and reproduction in populations. Natural selection refers to
the better survival and reproduction of some individuals, therefore more effi-
ciently transmitting their genetically determined characters, in given environ-
mental conditions (Darwin 1859). Environmental conditions are meant to
include everything outside the organism: the physical environment, the conspe-
cifics, the hetero-specifics, etc.
To document the role of natural selection and to validate the adaptive value of a
character are often considered as difficult subjects of study, especially in natural
conditions (Endler 1986). It necessitates documenting the survival and the repro-
ductive success of different individuals differing by different states of the putatively
adaptive character. The effect of natural selection is however inescapable, even if it
is difficult to study and if its importance cannot be known conclusively in advance.
A simple metaphor may help to understand the situation: individuals can be consid-
ered as objects of different size and shape put within different sieves with varying
degrees of coarseness. Passing (by survival and reproduction) through the sieve (the
environmental conditions) will have varying degrees of difficulty. At one extreme,
if the objects are much smaller than the sieve, there will be no filtering. A naïve
observer could claim that natural selection is not an explanatory concept. At the
other extreme, where objects are the same size as the holes in the sieve, filtering will
be of significant importance and the value of the concept will be obvious to any
observer. Thus, the occurrence of this sieve (the selective environmental conditions)
will be easier or harder to perceive depending on the intensity or the variance of its
effect. This does not mean that it is impossible to find some cases where characters
evolved without high direct selection (e.g., by neutral drift or by correlation/con-
straint with another character). It means rather that selection always acts fundamen-
tally and potentially. In other terms, for not validating adaptive assumptions which
are poorly documented or erroneous (type II errors, false positive), we must care-
fully avoid Type I errors (false negative) by refusing some correct adaptive assump-
tions too readily.
Based on all these considerations, it clearly appears that the complete study of
adaptation is a tough job, demanding studies pertaining to several scientific dis-
80 P. Grandcolas

ciplines (basically, phylogenetics and population biology) conducted at several

observational levels (clades and populations). In addition, the population studies
often do not consider the high diversity of possible situations in the field and
generalise the results obtained in a particular population to the clade5 or the
species.
Another important property of the concept of adaptation is to be relative to the
phylogenetic level of a given organism for which it is an evolutionary novelty.
Adaptation must be defined with strict reference to a species or a group of species.
If we ever refer to a group smaller than the one showing the apomorphy, we are no
longer dealing with an evolutionary novelty at this level. For example, vertebrae are
not an adaptation sensu stricto of mammals because they are a novelty for the ances-
tor of vertebrates, much anteriorly to the ancestor of mammals. They can still be
maintained by natural selection in mammals, but they are not their exclusive adap-
tive peculiarity. It can be said, rather, that mammals show an adaptation of
vertebrates.
Though operationally difficult to study, adaptation remains a concept central to
evolutionary biology because it is the sole explanation for the fit of organisms to
their environment. Organisms can evolve, change, but there are no reasons that
can explain a better functional fit except an adaptive process involving natural
selection. Neither neutral drift6 nor developmental constraints7 (Hall 1999), nor
genetic assimilation8 (Waddington 1953), nor more generally phenotypic plastic-
ity9 can explain, in isolation, why most organisms show features that look to be
shaped directly by the environmental mould and adjusted to a better survival. All
these kinds of process have often been misleadingly considered as valid alterna-
tives to the presumptive action of natural selection. But all these processes are
subordinated to the filter of natural selection, the action of which is ultimate and
unavoidable, even if potentially variable in terms of intensity and variance. To
sum up the situation, all organisms are genetically variable, and individuals with
different genetic features will be confronted by different situations of survival and
reproduction.

5
A clade is a group of taxa including a common ancestor and all its descendants. This is a mono-
phyletic group.
6
Process of genetic drift, when variation in frequencies and fixation of alleles are made by random
walk.
7
They are effects of the organisms’ structure in a developmental perspective (such as, amongst
others, the Bauplan, or organisation levels, inherited from a deep ancestor, for example the organ-
isational level of “vertebrates”).
8
Processes by which a phenotype initially produced in response to an environmental stimulus is
finally expressed genetically, independently of the stimulus action.
9
Variation of a trait caused by environmental changes.
5 Adaptation 81

2 The History of the Concept

Darwin formulated the theory of natural selection and he therefore determined the
importance of the concept of adaptation (Darwin 1859). The theory and that concept
have long been very popular: they are attractive and catchy. Etymologically, the
word “adaptation” clearly specifies a change – “ad” – toward a higher ability –
“aptus” and can only be confused with the reversible accommodation and pheno-
typic plasticity of organisms. It must be mentioned that the success of the concept is
partly due to the very misleading notion of evolutionary progress with which it has
been associated by some authors. According to this notion, life would “progress”
during the course of evolution, from most simple organisms toward more advanced
ones, on a ladder – a grade10 – of life where the species supposedly most evolved
and advanced would have accumulated more adaptations (unsurprisingly, Homo
sapiens is considered the most advanced!) It must be noted that Darwin himself was
clearly opposed to this gradist conception (Barrett 1960; O’Hara 1992) and that he
considered adaptation an explanation for the diversifying fit of the organisms to
their environment and not for a cumulative sophistication or advancement of
organisms.
The concept of adaptation, already much employed at the beginning of the twen-
tieth century, culminated in the 1960s, with general and famous presentations such
as Williams (1966). Such studies and theories were referred as to “adaptationism”
because they gave a central place to the concept of adaptation in evolutionary biol-
ogy. This term “adaptationism” sometimes became pejorative because some of
these adaptationist studies considered that showing characters were functional
“proved” that they were adaptive, without checking within the organisms or the
populations. Already at the beginning of the twentieth century, Morgan (1909) criti-
cised Darwinists who believed in defending the concept of adaptation by employing
it repeatedly as an ad hoc explanation in the case of characters that were simply
documented as fully functional. This “naïvely” adaptationist trend was still widely
found in recent studies that put an emphasis on the design or the optimality of the
traits (e.g., Thornhill 1990). Adaptationism was also accused of proceeding by tau-
tology according to the confusing locution of “survival of the fittest” put forward by
Spencer (cf. Krimbas 1984). This tautology was actually linked to a bad use of the
concepts of natural selection and adaptation. If organisms are considered globally,
without the details of their characters’ evolutionary histories, this principle is actu-
ally a tautology: if an organism is adjusted to its life conditions, its survival is gener-
ally better, and vice versa, building the tautology. In another way, if we consider a
specific phenotypic adaptation and its genetic heritability (which is, by definition,

10
A grade is a paraphyletic group (i.e. including an ancestor and some of its descendants only), an
invalid group in evolutionary biology and phylogenetic systematics. This kind of group is built on
the basis of a misleading assumption of evolutionary progress, together including taxa supposedly
primitive and evolved with regard to characters on which a focus is put.
82 P. Grandcolas

neither nil nor maximum), considering a “fit” to environmental conditions does not
imply survival in any case but a contribution to the fitness11 (Endler 1986).
The same criticisms that Morgan (1909) had about “naïve” adaptationism have
been formulated more recently in a famous paper by Gould and Lewontin (1979).
These latter authors argued in favour of a less teleological perspective in evolution-
ary biology, where the characters of the organism are not considered as necessarily
built “for” the adaptive value that can be guessed from a priori functional concep-
tions. In their famous metaphor, the spandrels of the San Marco Basilica were not
conceived by the architects for harbouring large paintings. On the contrary, the
arches of the church were conceived from the beginning as a support to the building
and they later provided an opportunity of ornamentation on their spandrels. This
less teleological conception of adaptation is reasonable, in that it has made more
clear for many that organisms, even if they look adjusted to their life conditions,
have inherited many characteristics (arches and spandrels), the function of which
has later been modified (from support to ornamentation). The organism is not “rein-
vented” with each generation but inherits many ancestral characteristics (the arches),
the use of which can be sometimes modified (ornamentation). This conception is
also involved in the term “evolutionary tinkering” used by some other authors
(Jacob 1977) and that means that organisms employ old things (characters) they
already have for building new functions.
Much older conceptions already followed the same rationale. Darwin (1859)
himself envisaged these kind of difficulties with the validation of his theory, and he
especially developed some thoughts in this respect in response to contradictors such
as Mivart. How to explain that complex organs – for example, vertebrates’ eyes –
could appear as very simple structures but are already adaptive enough to be main-
tained by natural selection and to allow subsequent complications. Darwin brought
the answer from the very first versions of the Origin of species (Tort 1997): struc-
tures can appear, therefore already exist and then only change for their function,
then complicate again, and change again with respect to their function, and also
possibly regress, etc. This question, and this answer, have even been commented on
and featured by fervent Darwinists such as Dohrn (1875), who saw them as one
more good reason to adopt the Darwinian theory of natural selection. Later, some
other authors again formulated the question and the answer, such as Davenport
(1903) or especially Cuénot (1909, 1914), who coined the term “preadaptation.”

3 Adaptation or Preadaptation and Exaptation?

Cuénot (1909, 1914) considered the difficulty mentioned by Darwin himself – the
origin of adaptations – and he concluded that the change of function could explain
that some structures are “preadapted”, facilitating subsequent evolution. According

11
Ability of a given phenotype to reproduce and transmit its genes, in given conditions.
5 Adaptation 83

to his papers, the conceptual difficulty is removed when the changes of function are
considered in the context of vacant niches (“les places vides dans la nature”).
However, the term of preadaptation has never been accepted unanimously. Fisher
and Stock (1915) strongly criticised it from the beginning, also accusing the “muta-
tionnist Cuénot” (!) to have a poor understanding of Darwin’s theory. It is true that
Cuénot’s contribution was made in the particular context of strong antagonism
between mutationnists and orthodox Darwinists. It is true also that Darwin (1859)
already mentioned function changes and vacant niches (see, for example, Lawton,
1982 for a modern formulation of this latter concept), as explanations useful for
understanding the origin of adaptations. The merit of Cuénot, if not of the more
orthodox Davenport (1903) sometimes cited as a promoter of that concept, is to
have coined a new term – preadaptation – that helps to take into account the func-
tional changes in an adaptive context. This term, even if it is always used one cen-
tury later, has never pleased the community, because its looks teleological, as if a
species was “fated” to be (pre)adapted.
This was probably the reason why Gould and Vrba (1982), following the ratio-
nale of Gould and Lewontin (1979) and Lewontin (1969, 1978), proposed the con-
cept of exaptation. They argued that this new concept valuably replaced the
preadaptation concept formulated in a teleological way. Gould and Vrba (1982) did
not cite, however, most of the literature on that question, eluding the contributions
of Cuénot (1909, 1914). They followed the same and very old tradition of the adap-
tive explanation by functional change. They took the birds’ feathers as an example,
which functioned ancestrally as a thermoregulatory device, before playing a role of
support and lift during flight. Gould and Vrba (1982) argued that characters could
acquire new functions that were added or substituted to previous ones, or even
occurred on a totally new basis. From this point of view, Arnold (1994) later created
a terminology relative to the functions of a trait, distinguishing between first use
exaptation, addition exaptation, and substitution exaptation. This concept of exapta-
tion has been more successful than preadaptation, probably because of it has been
elegantly formulated and it better fitted the political standards of the twentieth
century (Pigliucci and Kaplan 2000; Andrews et al. 2002). It has even been
used outside biology, in studies of cultural evolution, by linguistics or sociology
(for example, Botha 2002; Delius and Siemann 1998), as Gould (1991) himself
suggested. Even if the original formulation of exaptation implied that the concept
was aimed at replacing preadaptation, it is actually complementary, as shown by the
comparative analysis of Cuénot’s and Gould & Vrba’s works. Futuyma (1998)
clearly explained that preadaptation concerns the character with the original func-
tion, while exaptation concerns the character with its derived function (Fig. 5.2).
In the first case, the adaptation is seen as becoming, whilst in the second case, it is
considered in respect to its origin. In both cases, the emphasis is put on the history
of adaptation, with the need to consider adaptation as a modification of an ancestral
legacy and not only as a simple evolutionary novelty. This conception is more in
accordance with the nature of biological evolution, given that species inherit most
of their characteristics from their ancestors and only evolve a few.
84 P. Grandcolas

Fig. 5.2 The trait “A” can be

considered as either a
preadaptation or as an
exaptation with the
plesiomorphic function “1”
or with the apomorphic
function “2” respectively,
provided that the selective
value of the trait is measured
in each situation

An adaptive character appearing in the ancestor of a very speciose group may

be supposed to have strongly contributed to the evolutionary success of this group –
the radiation – especially if its sister-group12 lacking this adaptive character is much
less diversified: this is the concept of adaptive radiation. A hypothesis of adaptive
radiation is obviously highly speculative, depending on many auxiliary assump-
tions, including comparable extinction rates and sampling accuracy in both sister-
groups and the focus on one supposedly influential adaptation.

4 One Example and an Insightful Discussion: The Adaptive

Nature of Leaf Retention in Oaks

The literature is replete with examples of adaptive assumptions. However, few have
been studied in every phylogenetic or populational context or have been insightfully
discussed. One example is especially interesting from this point of view and concerns
leaf retention in deciduous trees in temperate areas, this phenomenon during which
most dead leaves remain on the tree after autumn and fall much later. In temperate
areas, everyone can see oaks covered with dead leaves in winter, long after other forest
trees have totally lost their leaves. Otto and Nilsson (1981) have proposed a possible
function for this retention in the family Fagaceae. The leaves of oaks have a petiole
lacking an abscission mechanism13 and they fall only after the mechanical break
of the dead petiole, therefore very late in the season. This delayed fall of leaves
allows the soil at the tree base to be enriched with nutrients very early in spring at
the time of tree regrowth. In the “usual” case of deciduous trees with leaf abscission
mechanism, the soil is enriched earlier in autumn and nutrients can be lost because
of weathering. This explanation based on experiments in oak populations referred
to an adaptive context. The function of the trait – supposedly adaptive – was
documented in a population, even if the selective value was not measured, strictly
speaking. Wanntorp (1983) strongly opposed the interpretation within this study,

12
Sister-groups are closer relatives to each other and they constitute an entire monophyletic group.
13
Cut of the petiole owing to a particular structure in the tissue, allowing the fall of leaves.
5 Adaptation 85

Fig. 5.3 The ancestor of the Fagacae was evergreen and the deciduous habit subsequently
appeared in species from temperate areas. Leaf retention (dead leaves remaining attached to the
tree during the cold season) may be considered an exaptation because the lack of petiole abscission
involved in leaf retention in deciduous oak species is inherited from an evergreen ancestor
(Modified from Wanntorp 1983)

putting forward that leaf retention is not an innovation in oaks (Fig. 5.3) but a
plesiomorphy14 inherited from a deep and evergreen15 ancestor in Fagaceae,
probably living in a tropical climate as are most present-day species of the same large
family. For example, this evergreen habit occurred in several Mediterranean oak
species. According to Wanntorp (1983), this phylogenetic context is contradictory
with the assumption of adaptation made by Otto and Nilsson (1981), because the
non-abscission of petioles is a plesiomorphic absence rather that an evolutionary
novelty per se in oaks. These two opposite conceptions, Otto and Nilsson (1981)
versus Wanntorp (1983), illustrate the necessary confrontation of both observation
levels needed for the study of adaptation. In this case, the confrontation between
these two conceptions was perceived as antagonistic. Actually, a synthesis between these
two studies is still compatible with an adaptive hypothesis sensu lato (Grandcolas
et al. 1994). In this way, the ancestral non-abscission may be considered as exaptive

14
Ancestral trait or character, not modified.
15
Trees whose leaves do not fall together seasonally.
86 P. Grandcolas

in the context of a seasonal temperate climate for these deciduous species of

Fagaceae. Non-abscission was perhaps even without any function at the origin
and it has later acquired an adaptive value in this new and particular context.
This hypothesis still depends on a real measure of the selective value of this trait in
oak populations, which is difficult to obtain and which is still lacking today.
This case study exemplifies how misleading it is to oppose the two observation
levels of clades and populations, both are necessary to carry out a powerful scientific
analysis. It also helps to understand how the traits of organisms need to be studied
within a historical perspective. This avoids considering that every trait is an adaptation
as soon as it looks functional.

5 A Few Conceptual Problems

Such a historical framework decoupling structure and function can look a priori
attractive because it allows one to get rid of naïve adaptationist conceptions
where organisms directly “solve” all of their problems under the action of natural
selection. This framework has, however, a conceptual limitation, sometimes men-
tioned but rarely discussed. Probably representing a large majority of researchers,
Coddington (1988 and pers. comm.) and Dennett (1998) argued that all innovations
are based on an ancestral legacy, even partial, and then concluded that there is no
reason for distinguishing amongst adaptation and exaptation. All adaptations would
actually be potential exaptations.
Several comments can be made in this respect. Firstly, this is difficult to affirm that
there is no true innovation that appears in the course of organism evolution when a
particular level of phenotypic integration is considered, for example, morphology or
behaviour (Müller and Wagner 1991). The genome may not show true novelties,
except with horizontal transfers,16 but some phenotypic characters may a priori be
considered true novelties (even if their genetic determinism has been modified from
an ancestral legacy). If we then admit that some true innovations actually occurred,
this will bring a conceptual paradox in which adaptations sensu stricto – representing
indeed the original concept – would be most uncommon and exaptations – a more
specific and derived concept – much more frequent.
Secondly, as already emphasised, the concept of exaptation and its less appreci-
ated companion – the preadaptation – allow one to consider adaptation sensu lato in
a historical framework that is still underemphasised. From this point of view, both
concepts need to be employed. If we share the opinion of Coddington (1988) or
Dennett (1998), why not simply consider exaptation and preadaptation as particular
cases of adaptation (aptation sensu Gould and Vrba 1982)?

16
Transfer of genetic material by other means that specific reproduction mechanisms and by cap-
ture of genetic material present in the environment (possibly interspecific); to be distinguished
from vertical transfers (sexual reproduction, pathenogenesis, scissiparity).
5 Adaptation 87

A much more important problem concerns the gap that remains unravelled
between the phylogenetic reconstruction documenting the origin of the presumptively
adaptive trait, and the populational study documenting the selective value of the trait
in a population at the present time. Even if the presumptive adaptation is actually an
apomorphy in the taxon considered, even if this trait actually confers high fitness in
one or two present populations, it will still remain unknown whether this trait has,
strictly speaking, been adaptive from the time of its origin to the present-day popu-
lations (Grandcolas and D’Haese 2003). Some authors focused on this gap and
argued that history does not matter and that we should redirect all our attention to
study the present populations (Reeve and Sherman 1993). With such an opinion,
they overlook the fact that phylogenetic analysis allows one to ask the right ques-
tions by setting the evolutionary study’s background.17 Very often, the question
asked at the beginning of such a study is not appropriate: for example, to study how
parental investment can explain the extreme sexual dimorphism by the decrease of
the body size – presumptively adaptive – of males of Nephile spiders is nonsensical
since phylogeny shows us that females have increased their size and that males did
not actually increase in size (Coddington et al. 1997).
To fill the gap between phylogeny and population studies, some authors have
searched to take the effect of natural selection at the level of phylogenetic analysis
into account (Baum and Larson 1991). On this scale, a “selective regime” would be
substituted to the real measure of the natural selection in populations. According to
the examples cited by these authors, this regime corresponds to using presumptively
adaptive characters, the history of which would also be reconstructed onto the phy-
logenetic tree. Tarsal structures in lizards have been considered this way, by putting
them into relationships with the kind of movement performed by the animals and
the kind of substratum on which the animals move. The use of such attributes on a
phylogenetic tree represents a very poor surrogate for measuring the selective value.
This value is not measured in terms of differential survival and reproduction but in
terms of use or performance with a trait. In addition, this method is supposed to
reconstruct the phylogeny of this approximated selective value. The main problem
there is that natural selection is an environmental context, not an organismic char-
acter, and therefore it is not heritable. To analyse its evolution on a phylogenetic tree
is thus nonsensical (Grandcolas and D’Haese 2003). In addition, a character, even
very functional, does not necessarily have a high selective value. This is the problem
of optimality studies (Thornhill 1990) that consider that a good design and a perfect
optimality are strong indications of adaptation. This is the teleonomic domain of the
study of adaptation that claims philosophical legitimacy: every function is assumed
to necessarily have a purpose as indicated by the quality of its design or it efficiency
(for example, Griffiths 1993; Crespi 2000).
In this context, the study of the purpose of the adaptive fit of a trait comes to
guess which function has been the target of the natural selection. The problem is
that this guess, especially when it is made without a phylogenetic context, is nothing
other than an ad hoc history (the “just so stories” after S.J. Gould, borrowing from

17
Wanntorp (1983), Coddington (1988), Carpenter (1989), Grandcolas et al. (1994).
88 P. Grandcolas

Rudyard Kipling). This is just the modern and sophisticated continuation of the
adaptationist tradition from the early twentieth century. From this point of view,
evolutionary biology should learn how to characterise the uses of a trait without
assuming a function as essential from ethology: ethologists have long understood
that a morphological structure can be used in several ways by an organism in a
behavioural context, without considering that one amongst these uses is purposely
functional.
Another abuse of the adaptation concept concerns the so-called “comparative
method”, a very specific term for a particular branch of comparative biology that
pretends to detect adaptation by the study of convergence.18 The “adaptationist
wager”, according to Pagel (1994) and borrowing from Pascal, acknowledges adap-
tation by assessing a recurrent association between a character and a role in varied
taxa (for example, warning coloration, gregariousness and aposematic defence19 in
butterflies – cf. Sillén-Tullberg 1988). This association will be statistically evaluated
on phylogenetic trees. This adaptationist bet does not take into account the popula-
tional dimension of the study of adaptation. It also misunderstands that a functional
character and efficiently functional is not necessarily a novelty at the considered
taxonomic level, nor does it favour the fitness of the organism. Leroi et al. (1994)
have presented a complete list of criticisms of this adaptationist bet, showing that
convergence can be caused by many confounding factors, such as genetic linkages or
trait architectures. In addition, a fundamental problem of the comparative method
(and especially of the “phylogenetic correction” method) is that it considers phylog-
eny as a source of statistical error because of non-independence among the compared
species (Coddington 1994). This method limits itself to evaluating the real size of
samples in terms of independent taxa used in species comparisons. To compare sev-
eral groups of closely related taxa would only compare their common ancestors,
significantly less than the number of taxa, and therefore decreasing the number of
degrees of freedom (Clutton-Brock and Harvey 1979). The so-called “phylogenetic
correction” also ignores the many different and detailed evolutionary histories that
allow for a better understanding of the context of adaptation evolution (Wenzel and
Carpenter 1994). This is the reason that it has become less and less employed by
comparison with detailed phylogenetic analysis.
As a matter of statistical analysis of data and generalisation of results, for the test
of adaptational hypotheses it would be much more interesting to control the biases
occurring according to the selection of phylogenetic case studies. Do the clades stud-
ied until now correctly sample the Tree of Life (Guyer and Slowinski 1995; Grandcolas
et al. 1997)? This question can be answered by looking at the topologies of the groups
studied. For example, the study of small clades will prevent taking the possibility of
radiations that can be detected only by considering large clades into account.

18
Adaptive convergence means that unrelated species present adaptations functionally similar but
that appeared independently during evolution (for example, the wings in bats and in birds). See
Clutton-Brock and Harvey (1979), Felsenstein (1985), Harvey and Pagel (1991).
19
It is said from the appearance of animals advertising a potential predator that it is dangerous to
eat them (e.g., toxicity).
5 Adaptation 89

6 When There Is no More Adaptation: Maladaptation

or Desaptation

The notion of maladaptation or desaptation (Baum and Larson 1991; Crespi 2000)
is not often employed. It probably suffers from the difficulty of qualifying nega-
tively and of being characterised by a lack or an absence. Indeed, an organism is
said to be maladapted or desadapted with respect to a specific trait if it decreases the
fitness of, but is maintained, in that organism. The novelty of that trait or its function
is not a defining criterion as in the case of adaptation. On the contrary, a desaptation
is diagnosed by reference to a previous state in the course of evolution, in which the
trait and its function already existed and increased the fitness. To demonstrate this,
a quantitative genetic study should be performed on the supposedly maladapted spe-
cies and on a related species showing the ancestral state still “adaptive”, thus within
a phylogenetic framework. This way, a hypothesis of maladaptation could be vali-
dated by showing the contribution of a trait to the fitness which apparently becomes
negative in the course of evolution.
Some other less complete and more disputable approaches have also been pre-
sented. According to Baum and Larson (1991), the present sub-optimality of the
supposedly maladaptive trait is a hypothesis corroborated by its lower performance
compared to the ancestral state. This again relies on the notion of the performance/
selective regime, as a misleading approximation of the selective value. Many authors
have also proposed some teleological approaches that basically assume that all
selected traits are a priori optimised and that maladaptation can therefore be diagnosed
as an exception to these optimal situations. In that context, a theoretical functional
study allows one to assess that the trait is not optimised, on the basis of an optimality
criterion referring to energy, metabolism, functional morphology, etc.
A maladaptation or a desaptation is not necessarily a vestige or a regression,
contrary to a common misunderstanding (concerning vestigial traits, cf. Griffiths
1992). A trait can be lost or have regressed in the course of evolution, specifically
under the effect of natural selection: in this case, the trait optimally fits because setting
up a non-functional trait saved some energy (or any other functioning cost) when
the function was no longer essential to the survival or the reproduction, at least with
the same development or intensity of functioning. On the other hand, if the function
of the vestigial trait has not changed, the same true adaptation may still be at work
even with a vestige, contrary to any other a priori assumption. If the function has
been lost with that regression, the trait can be said to be non-functional and thus
ipso facto a non-aptation. To actually be maladaptive, a vestige issued from a
regression should negatively contribute to the fitness.
Another notion often related to maladaptation is the “constraint.” It has, however,
become a vague term (Antonovics and van Tienderen 1991), to the extent that many
authors refuse to employ it (for example, Crespi 2000). Concerning the specific case
of maladaptation, the notion of constraint can be employed if we consider an organ-
ism maladapted, for example, because of an inherited ancestral character contribut-
ing negatively to the fitness. The maladaptive trait is hence considered to constrain
the organism.
90 P. Grandcolas

7 Conclusion

Unlike Gould and Lewontin (1979), we do not hypothesize that many traits are not adaptive.
Rather, we are making the case that adaptive (or nonadaptive) nature of traits cannot be
determined from most comparative data (Leroi et al. 1994: 397).

If the debate concerning the use of the concept of adaptation has to be sum-
marised in one sentence, it can be said that it is invaluable to evolutionary biology
but difficult to study in practice. As showed by the epigraph above, discussions
about adaptation are often marked by strong opinions a priori: I am or I am not
adaptationist, I believe or I do not believe that comparative biology brings decisive
information in this respect. Rather than making such strong a priori arguments, we
would do better to analyse the data in the strictly defined and well-made method-
ological framework of recent decades. This appropriate methodological framework
allows us to carry out the scientific study of adaptation by putting several different
disciplinary fields, phylogenetics and population biology, in conjunction. Some see
it as an operational difficulty but instead this is a great opportunity to carry out a
very heuristic scientific approach and an interdisciplinary synthesis. The phyloge-
netic analysis of the presumptively adaptive traits is a remarkable opportunity to set
up the historical background knowledge for the adaptational study and to under-
stand what a case study can actually teach us. That way, the polarity and the number
of changes can be inferred for the considered trait, allowing an understanding of
why functional or populational studies sometimes totally fail to reach their aim
(Grandcolas et al. 1994; Coddington et al. 1997). The theoretical justification of this
methodology, considering both phylogenetic and populational evidence, also shows
how useless it is to employ shortcuts. Some authors have attempted to get rid of
phylogenetic studies (Reeve and Sherman 1993) or from populational studies, either
with the comparative method that disputably equates convergence and adaptation
(Harvey and Pagel 1991), or with methods aimed at detecting a supposedly adaptive
optimality.
The absence of one of those two kinds of study – phylogenetic or populational –
makes the adaptive assumptions less corroborated and brings about some doubts as
to the general value of the concept in the long term. In this context, it really is inap-
propriate to claim to be for or against adaptationism a priori, which can only bring
about important biases in case studies.

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Philippe Grandcolas Senior Scientist CNRS. Head of the CNRS laboratory “Institut de
Systématique, Evolution et Biodiversité” that includes most of the systematists at the Muséum
national d’Histoire naturelle of Paris. His studies focused on phylogenetic analysis of evolution,
with a special concern for the origin of phenotypic traits and insular biota.

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