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Biological Journal of the Linneun Society (2001), 72: 509-517. With 2 figures
doi: lO.lOOS/bij1.2000.0512, available online at http;//www.idealibrary.com on
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Evolutionary stasis, constraint and other
terminology describing evolutionary patterns
D. BRENT BUW
Department of Biology, Stephen l? Austin State University, PO. Box 13003, SFA Station, Nacogdoches,
Texas 75962-3003, USA
Received 3 March 2000; accepted for publication 20 December 2000
Current use of terms to describe evolutionary patterns is vague and inconsistent. In this paper, logical definitions
of terms that describe specific evolutionary patterns are proposed. Evolutionary inertia is defined in a manner
analogous t o inertia in physics. A character in a static state of evolutionary inertia represents evolutionary stasis
while a character showing consistent directional evolutionary change represents evolutionary thrust. I argue that
evolutionary stasis should serve as the null hypothesis in all character evolution studies. Deviations from this null
model consistent with alternative hypotheses (e.g. random drift, adaptation) can then give us insight into evolutionary
processes. Failure to reject a null hypothesis of evolutionary stasis should not be used as a serious explanation of
data. The term evolutionary constraint is appropriate only when a selective advantage for a character state
transition is established but this transition is prevented by specific, identified factors. One type of evolutionary
constraint discussed is evolutionary momentum. A final pattern of evolutionary change discussed is closely related
to evolutionary thrust and is referred to as evolutionary acceleration. I provide examples of how this set of definitions
can improve our ability to communicate interpretations of evolutionary patterns.
02001 The Linnean Society of London
ADDITIONAL, KEYWORDS: evolutionary acceleration - constraint - effects - inertia - momentum - stasis thrust.
INTRODUCTION
“he last two decades have seen a dramatic increase in
the use of phylogeneticallybased comparative methods
(Brooks & McLennan, 1991; Harvey & Pagel, 1991).
These methods often examine hypotheses of adaptive
evolution and the ecological contexts of evolutionary
change. Such hypotheses must be tested in a phylogenetic framework because species evolve in a hierarchical framework and cannot be used as independent
data points (Felsenstein, 1985;Maddison & Maddison,
1992). Some comparative methods control for these
‘phylogenetic effects’ so that appropriate statistical
comparisons on trait variation can be made (Cheverud,
Dow & Leutenegger, 1985; Felsenstein, 1985; Harvey
& Pagel, 1991). Other ‘tree thinking’ methods make
direct use of phylogenies t o reconstruct hypotheses
of character state evolution (Maddison & Maddison,
1992). Adaptive hypotheses are tested by examining
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the pattern of gains and losses in these characters as
they relate t o the presumed ecological context of each
change. Researchers may find some evidenceto support
their adaptive hypotheses, but in most cases the pattern is not perfect. Often, phylogenetic effects are
offered as explanations for deviations from expectations of the adaptive model.
The term phylogenetic effects is used in two different
contexts above and while most evolutionary biologists
have a basic understanding of this term, we need t o
be more specific in our use of such terms. Other terms
in use that represent the general class of phylogenetic
effects include phylogenetic or evolutionary inertia,
evolutionary stasis, phylogenetic or evolutionary constraints, developmental constraints, and genetic constraints. Unfortunately, these terms are often vaguely
defined, if at all. In some cases the terms simply
describe evolutionary patterns, while in others they
imply underlying processes. Lack of definition and
loose usage is the primary reason for the negative
feelings held by some biologists toward these terms
(Antonovics & van Tienderen, 1991; Leroi, Rose &
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0 2001 The Linnean Society of London
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D.B.BUW
Lauder, 1994). We badly need to begin associating
different evolutionary patterns with consistent, appropriate terms.
Evolutionary effects terms are important and should
be used in meaningful ways in evolutionary studies.
Previous authors (Maynard Smith et al., 1985; Ligon,
1993; McKitrick, 1993) have reviewed many of the
patterns and possible processes associated with evolutionary effects terms. I revise and expand on these
interpretations of evolutionary effects terms and clarify how they should be used in character evolution
studies. Specifically, I describe the logical basis for a
more explicit definition of the most fundamental of the
evolutionary effects terms, evolutionary inertia (EI),
and why this term should be replaced in most cases
by the terms evolutionary stasis (ES) and evolutionary
thrust (ET). I then outline why ES should serve as the
null model of evolution in comparative studies. Next,
I delineate ES from the term evolutionary constraint
(EC) and outline the restricted ways in which we
should use the latter term. I then introduce and define
two additional terms, evolutionary momentum (EM)
and evolutionary acceleration (EA).
DEFINITIONS OF INErtTIA
Before deriving a definition of EI we should examine
inertia’s initial usage. In physics, Newton’s first law
of motion defines inertia. The law of inertia states: a n
object a t rest will remain a t rest and a n object in
uniform motion in a straight line will maintain that
motion unless a n external resultant force acts on it
(Serway & Faughn, 1985). The key concept here is
that a n object does not change its state unless forced
to do so by a n external force.
I have derived a definition of EI that is parallel to
the law of inertia: a character with an unchanged
character state will remain unchanged and a character
experiencing consistent directional change will maintain that evolutionary pattern between generations of
a lineage unless an external resultant force acts on it.
However, in comparative studies we are unable to
track evolution at each generational stage and therefore must have another, operational definition: a character with an unchanged character state will remain
unchanged and a character experiencing consistent
directional change will maintain that evolutionary pattern between branches of a phylogenetic tree unless
a n external resultant force acts on it.
These definitions of EI point out two possible inertial
states. The first part of each definition simply states
that without a resultant change in the forces of mutation, selection o r drift, genetic change cannot occur. In
this sense, EI describes evolutionary stasis, which
fits the common usage of this term. However, can
characters have other inertial states that fit the second
part of the definitions above? Are there characters that
can show consistent directional change as the state of
inertia (e.g. DNA sequence divergence under neutralist
conditions)? If so, we need to distinguish between
characters that show EI as stasis and those that show
EI as change. The former I will refer to as evolutionary
stasis (ES), which again is the most intuitive usage of
the term EI. The latter I will refer to as evolutionary
thrust (ET). Since EI can take two very different forms
I feel we should not use the term EI in most situations
and should instead use ES and ET in the appropriate
circumstances. I now explore the appropriate use of
ES in comparative studies and will return t o discuss
ET.
I contend that the concept of ES, or static EI, should
serve as the appropriate null model for character evolution studies in which one hopes to study the mechanisms of evolution. This null model simply states that
heredity works. Traits are passed on from generation
to generation in a lineage unless forced to change.
For example, the phylogeny in Figure 1 A shows the
extreme of ES for the character traced. A trait may
remain even if it is no longer of any use (a ‘secondary
nonaptation’ Baum & Larson, 1991). In this case the
term ES simply describes a pattern and implies no
process. However, it is important to realize that a
character that shows a patterns of ES may be under
stabilizing selection as a n operating factor maintaining
the character state (Ridley, 1983). That is, ES may be
maintained by selection, but selection is not necessary
to maintain ES. My definition of ES does not rule out
evolutionary forces as a whole, it merely states that
there are no resultant evolutionary forces that would
result in change.
A parallel example again from physics may make
this point clear. The binoculars on my desk will remain
stationary until moved. Their static, inertial state will
persist unless external resultant forces come into play.
However, the concept of inertia does not mean that
external forces are not currently acting on the binoculars. Gravity is exerting a downward force on the
binoculars and the desk is exerting an equal and
opposite force. Gravity, however, is not required t o
keep the binoculars in this static state. If we could
somehow suspend gravity they would stay in place. In
a similar manner, a hypothesis of selection is simply
a n additional hypothesis that can coincide with the
null hypothesis of ES. Stabilizing selection may be
maintaining a certain character state in each of the
taxa represented in a phylogeny. The burden of proof
for this additional hypothesis of adaptation is simply
on the shoulders of the investigator. Prum (1994) discussed this point in his examination of the patterns of
evolutionary stasis in lekking and cooperative displays
of manakins.
As mentioned above, the phylogeny in Figure 1A
EVOLUTIONARY PA’ITERN TERMINOLOGY
B
C
D
E
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Figure 1. Differing degrees of evolutionary inertia. The character mapped in each phylogeny on the top row shows
either: (A) complete stasis, with no evolutionary change; (B) intermediate stasis, with some transitions but not so
many as to make the reconstructed evolutionary pattern unreliable; or (C) no stasis, with a high rate of evolutionary
transitions such that the evolutionary pattern is randomized. The character mapped in each phylogeny on the bottom
row shows consistent, directional evolutionary change representing either (D) slow or (E) fast evolutionary thrust.
shows the extreme of ES for the character traced. Of
course there will be differing degrees or numbers of
phases of ES in different characters (intermediate EI,
Fig. 1B). Accordingly, not only is ES a n appropriate
null model, but the degree of ES is a n important
determinant of how appropriate it is to trace a character onto a phylogeny in the first place. In fact, it is
an implicit assumption in all character evolution studies that the mapped characters must have some ES to
have a pattern of transitions that can be accurately
reconstructed. Taken one step back, ES is the reason
phylogenies can be reconstructed in the first place.
Of course, continuous change in variable directions
represents a complete lack of EI and therefore provides
no evolutionarily reliable information (Fig. 1C).
On the opposite EI extreme are characters that
change every generation. Continuous change in a consistent direction every generation fits extreme ET (Fig.
1E). A trait in ET is evolving under the influence of
some consistent evolutionary force(s) and will continue
to do so until there is a resultant change in evolutionary
forces. An example of ET is neutral DNA sequence
divergence. Under the neutralist model, DNA sequence
divergence is due to relatively continuous fixation of
neutral mutations by drift. In fact, ET underlies the
reasons for calculation of a DNA clock. Additionally,
the rate a t which the clock ticks is due to the rate of ET
(Fig. lD, slow clock; Fig. lE, fast clock). Evolutionary
patterns in runaway sexually selected traits driven by
female choice may also fit ET (Prum, 1994). Evolutionary thrust is also evident in the gradual reduction
of vestigial appendages.
INTERPRETING EVOLUTIONARY STASIS
As I’ve outlined the term above, I argue that most of
us already operate with ES as our unspoken null model
in comparative studies. Unfortunately, the term is
typically used in the literature only when a researcher
fails to see a perfect match between evolutionary patterns and a n expected pattern of adaptive evolution
(Antonovics & van Tienderen, 1991). For example,
consider a hypothetical case of egg pattern evolution
as it relates to nesting in either cavities or in open cup
nests (Fig. 2). The adaptive expectation is that spotted
eggs should evolve in open cup nests for camouflage.
The pattern of egg-colour evolution doesn’t conflict
with this adaptive scenario, but it does not completely
match either. We see the delayed evolution of spotted
eggs within each open cup nesting clade. Also, we don’t
see the loss of spotted eggs in the absence of selection
pressures for camouflage when one lineage returns to
cavity nesting. There are two ways in which we could
interpret this pattern.
In one interpretation we could say the null model of
ES could not be rejected in all sections of the tree, but
when we do see change the alternative hypothesis of
adaptive evolution is supported. We could then use a
test, such as the concentrated-changes test (Maddison,
1990), to quantify the strength of support for the
alternative hypothesis. This interpretation is what I
recommend.
However, another interpretation is likely to be found
in the literature: The adaptive explanation has some
support but fails to match completely due to the ‘force
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D.B.BURT
once and then persisting for extended periods of time
(Winkler & Sheldon, 1993). Each of these examples
describes a character evolution pattern with little or
no change. In each example, the genetic basis of each
trait is the only assumption needed t o explain the
pattern, no process other than heredity is required.
DISTINCTIONS BETWEEN EVOLUTIONARY
Spotted Eggs
Nest Type:
I
Open Cup
Figure 2. Hypotheticalcase of eggshell pattern evolution
as it relates t o open cup or cavity nesting. The pattern
reconstructed only partially matches the adaptive expectation that spotted eggs should evolve in open cup
nesting species. Two interpretations of this pattern as it
relates to evolutionary stasis are discussed in the text. A
pattern of evolutionary constraint is supported if starred
taxa have genetic constraints that hinder the evolution
of spotted eggs.
of phylogenetic inertia’. In this case, the operating
hypothesis is built on an adaptive framework and ES
ends up being the alternative explanatory hypothesis
(‘origin, not maintenance”, Coddington, 1988). The
differences between these two interpretations are
subtle but important. The latter case puts the cart
before the horse and is an inappropriate use of ES. We
should use evolutionary patterns t o study adaptation,
not assume adaptive evolution as the force that always
moulds evolutionary patterns (Gould & Lewontin,
1979). This ad hoc use of ES also explains most of
the negative feelings many biologists have toward
evolutionary effects terms. By using my preferred interpretation we are stating that we should only get
excited when there i s a demonstrable lack of ES which
is consistent with our alternative adaptive hypotheses.
Numerous studies describe evolutionary patterns
consistent with ES. Certain tropical trees have fruits
that are too large and hard for effective animal dispersal. These fruits are likely evolutionary holdovers
from a time in which now-extinct large mammals once
served as effective dispersal agents (Janzen & Martin,
1982).These fruits are in a state of ES and will remain
so until changed by the resultant evolutionary forces
of mutation and selection. No process is needed t o
explain the persistence of these fruits. Cooperative
breeding in Aphelocoma jays also fits a pattern of
ES (Peterson & Burt, 1992). Cooperative breeding
behaviour likely evolved early in the diversification
of this genus and persists in many lineages despite
significant ecological change. Swallow nest building
behaviour shows a high degree of ‘evolutionary conservatism’ with each nest type having evolved only
STASIS AND EVOLUTIONARY CONSTRAINT
Diniz-Filho, de Sant’Ana & Bini (1998) initially describe phylogenetic inertia in a manner consistent with
ES but then go on t o explain how it is maintained
by various mechanisms. In other words, they imply
process behind the pattern. They describe phylogenetic
inertia as character similarity among closely related
species. They claim this similarity can be explained
by *. . .niche conservation, time lags on evolutionary
processes, and phenotype-dependent responses to selection” (Diniz-Filho et al., 1998: 1248; citing Harvey
& Purvis, 1991). In cases where ES is used to explain
negative results, researchers often imply that vague
mechanisms have prevented evolution from occurring.
These interpretations of phylogenetic inertia oppose
my use of ES as a null model for character evolution
that assumes a lack of resultant evolutionary mechanisms. However, time lags and lack of genetic variation are often implied as constraining mechanisms
in the literature (Maynard Smith et al., 1985; Harvey
& Pagel, 1991; McKitrick, 1993; Diniz-Filho et al.,
1998).These factors are not in themselves constraining
mechanisms but may be indicative of other constraining factors (see below).
This typical tie between ES and mechanisms leads
t o its confusion with another term: EC. Unfortunately,
many authors treat these and similar terms, at least
at times, as synonyms (Maddison & Slatkin, 1991;
Ligon, 1993; McLain, 1993; Kusmierski et al., 1997).
This paper will not present a major review of EC (see
Maynard Smith et al., 1985; Ligon, 1993; McKitrick,
1993). I will instead explain how ES and EC differ.
Evolutionary constraint has been defined as . any
result o r component of the phylogenetic history of a
lineage that prevents an anticipated course of evolution
in that lineage” (McKitrick, 1993: 309). I agree with
McKitrick (1993) that EC is an important term whose
use can help us understand mechanisms limiting specific evolutionary patterns. In cases of EC, an evolutionary pattern of ES is seen due t o underlying
constraining processes. However, before EC can be
identified two conditions must be met. First, a selective
advantage for a character state change must be established (Blackburn & Evans, 1986; Berger, 1988).
Second, specific factors o r mechanisms hindering this
transition must be identified (McKitrick, 1993).Traits
under EC are prevented from reaching clearly defined
#..
EVOLUTIONARY PAlTERN TERMINOLOGY
adaptive peaks relative to specific traits. A trait showing a general pattern of ES due to mechanisms constraining specific adaptive evolutionary patterns fits a
pattern of EC. Currently, the term EC is often used
in the absence of a known mechanism (Derrickson &
Ricklefs, 1988). By inferring EC, one does not mean
that the constraints cannot be overcome, only that
there is a specific obstacle or set of obstacles that
at least temporarily prevent expected evolutionary
change.
I see three primary classes of EC mechanisms: adaptive trade-offs, developmental constraints and genetic constraints. However, identification of constraint
mechanisms and distinctions between the three constraint classes are not always clear (Maynard Smith
et al., 1985; McKitrick, 1993). Adaptive tradeoffs are
indicated when selection on one trait prevents adaptive
evolution in another trait (Gould & Lewontin, 1979).
Developmental constraints can be due to a variety of
factors including allometry, Von Baer’s laws, bauplan
restrictions, and structural restrictions (Gould & Lewontin, 1979; Maynard Smith et al., 1985; Wagner,
1995). Genetic interaction constraints such as epistasis
and pleiotropy can exist; however, too often genetic
constraint arguments are used in the absence of evidence for specific genetic constraining mechanisms
(Leroi et al., 1994). Lack of genetic variation is not a
mechanism of EC; it is ES until you can demonstrate
mechanisms preventing the mutational variants from
forming.
When should we look for EC? This step should begin
when we fail to reject ES in a study. Failure t o reject
the null model should lead to examination of possible
EC mechanisms. Returning to the egg pattern evolution example, further analyses may find evidence of a
pleiotropic gene controlling both egg colour and egg
shell thickness in the taxa marked with stars (Fig. 2).
A mutation for spotted eggs also results in shells being
of the wrong thickness and provides a constraint to
adaptive evolution in these lineages. Additionally, we
may find that gene duplication events have allowed
for the independent expression of genes responsible
for egg colour and eggshell thickness in the remaining
open-cup nesting taxa (those without stars). Release
from genetic constraints has allowed these lineages
to evolve spotted eggs in the appropriate ecological
contexts. Assuming that we have evidence that spotted
eggs would be an adaptive advantage in the constrained taxa, possibly through experimental studies,
we now meet the two conditions needed to claim EC
is involved in portions of this clade. Evolutionary constraints may be common; however, until these two
conditions are met the evolutionary pattern should be
interpreted as nothing more than ES.
Examples of EC in the literature do exist in which
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both the selective advantage of change and the constraining factors are identified. Palms may be constrained from branching because they lack secondary
tissue (Maynard Smith et aZ., 1985). The lack of viviparity in birds has been a long-standing mystery in
ornithology. The conditions needed for viviparity t o
be an advantageous life history strategy are limited
(Blackburn & Evans, 1986) but the trait may also be
evolutionarily constrained by high oviduct temperature and low oviduct oxygen levels (Anderson,
Stoyan & Ricklefs, 1987). Cavity nesting coraciiform,
piciform and trogoniform birds may be evolutionarily
constrained from open-cup nesting due to thermoregulatory limitations, slow developmental rates, and
poor nest hygiene that would likely attract predators
to open-cup nests (Ligon, 1993). Multinest polygyny
cannot evolve in cuckoos and woodpeckers as long as
male-only nocturnal incubation occurs (Ligon, 1993).
Sexual selection may constrain evolutionary patterns
in certain mammal and bird lineages. Runaway selection for large males in mammals may drive the
population’smean body size off its adaptive peak. This
EC may help explain the high extinction rates of
mammal lineages (McLain, 1993). In manakins, and
possibly other lekking species, the ECs of female preference for elaborate lekking displays may limit the
evolution of biparental care in appropriate ecological
circumstances (Prum, 1994). Iguana tongue evolution
is limited by efficient prey capture morphologies and
constrains the evolution of chemoreception (Schwenk,
1995). The fact that wheel appendages have never
evolved is an example of an EC that is likely never
to be overcome due to problems of innervation and
circulation.
Many authors, however, fall into the trap of claiming
EC without evidence for constraining mechanisms.
Elongated bodies are selectively advantageous in fossorial salamander species. Wake (1991) claims that a
lack of genetic variation for increasing vertebral number in the genus Lineatriton prevents one route to this
adaptive morphology. Wagner (1995) evokes ECs as
preventing the evolution of certain shell morphologies
without reference to specific constraining factors. The
interpretation in each of these studies should be ES
until shown otherwise. Ligon (1993) at times uses EC
as a synonym for a variety of evolutionary patterns.
Clutch size in Lams gulls, paternal-only parental care
in ratites and tinamous, and cooperative breeding in
some bird lineages should all be interpreted as ES
with the available evidence.
EVOLUTIONARY MOMENTUM
I now assign a term to an evolutionary pattern that
has been recognized for some time as a form of EC.
Ligon (1993: 3) best described this phenomenon:
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D. B. BURT
". . . certain evolutionary pathways are not likely to be
followed by a species or group of related species as a
result of prior evolutionary history. In short, yesterday's adaptation, may be today's constraint". I assign
the term evolutionary momentum (EM) to this phenomenon. Evolutionary momentum can be considered
a subcategory of EC. Evolutionary momentum is related to physical momentum. In physical momentum,
mass is the determining factor of how difficult it is to
change the trajectory of an object. In EM, the extent
and direction of past trait evolution is analogous to
mass in physical momentum. The more EM, the more
difficult it may be to change a trait into another specific
trait form. Evolutionary momentum makes certain
transitions unlikely, a t least for a n extended time. The
evolutionary forces that have driven a trait up one
adaptive peak may greatly reduce the future paths
by which the trait can evolve. Species' traits become
isolated from alternative adaptive peaks (Riedl, 1978;
Maynard Smith, 1985).
A trait that has undergone extreme specialization
is likely to have a great deal of EM. Nest building
behaviour is unlikely to evolve in both megapodes
(Ligon, 1993) and obligate brood parasites due to EM
created by adaptations for their current breeding systems. Morphological evolution for a n arboreal life style
may be limited in white-cheeked mangabeys (Lophocebus albigena) due to morphological specializations for terrestrial locomotion in its ancestors
(Nakatsukasa, 1996). In a similar manner, humans
are not perfectly adapted to bipedal locomotion due to
our quadrapedal ancestry (Gould & Lewontin, 1979).
Maintenance of cooperative breeding behaviour in
some bird lineages may be due a t least partially t o
EM. Clades with cooperative breeding species show
very few reversals to non-cooperative breeding (Peterson & Burt, 1992; Edwards & Naeem, 1993). Helping behaviour is a life history alternative for young
birds that in some ecological situations increases their
lifetime reproductive success. In this sense, helping
behaviour is an ecological specialization. Once helping
behaviour has evolved it may prove costly to reverse.
Even if the selective advantages for helping behaviour
no longer exist it may work against the long-term
fitness of helpers to evolve the ability to refrain from
providing alloparental care. Genetic changes that
would allow helpers to ignore the sounds of begging
young might also make them less effective parents
once they become breeders (Jamieson, 1989; Ligon,
1993).However, until a genetic constraint can be identified, this pattern in cooperative breeding clades
should be considered ES. The prior examples of sexually selected traits in large mammals and lekking birds
might also be considered examples of EM as a subclass
of EC.
EVOLUTIONARY ACCELERATION
One additional potential evolutionary pattern needs
discussion. Do certain traits show increasing rates of
evolutionary change through time? That is, do they
accelerate? If so, evolutionary acceleration (EA) seems
to be a n appropriate term to describe this pattern.
Evolutionary acceleration is a form of ET in which
change between successive character states is increasingly amplified or the time interval between successive character state changes is reduced. Maynard
Smith et al. (1985) hint a t this possibility when discussing the evolution of selfish DNA content in organisms. As copy number of selfish DNA elements
increases so do the chances that additional copies will
be created due to more frequent meiotic errors. Early
stages in the evolution of sexually selected ornaments
might also show accelerated elaboration fitting a pattern of EA. Another potential pattern of EA may be
seen in the adaptive radiation of lineages. Do traits
associated with adaptive radiations show EA? Does a
clade whose lineages show ever-increasing ecological
and/or behavioural specialization fit a pattern of EA?
Documenting such patterns is no easy task. However,
if such patterns of EA can be identified and generalized
to certain biological situations we may then develop
more detailed models of character evolution. These
models will then allow the reconstruction of more
reliable ancestral character state assignments
(Schluter et al., 1997).
CONCLUDING REMARKS
If we are to accurately describe evolutionary patterns
we must first have appropriate, precise terms. Many
of the studies cited here used evolutionary effects terms
inappropriately, a t least as I've defined them here.
However, to be fair, each of these authors was working
in a terminological quagmire. I have attempted to
provide more explicit definitions to evolutionary effects
terms in common usage and to new terms that are
needed to describe other evolutionary patterns that
we attempt to describe and interpret (Table 1).
Evolutionary stasis is the most basic of the evolutionary effects terms discussed here. I argue that ES
should serve as the null model in comparative studies.
Evolutionary stasis is based on the concept that traits
do not change in a n evolutionary vacuum. Antonovics &
van Tienderen (1991) suggest that null models should
assume evolutionary change. They claim models
should be based on an explicit mechanistic evolutionary
framework and alternative explanations should outline
factors that constrain the expected pattern. I claim a
null model used to study evolution should not assume
evolution. Some may balk a t this suggestion. After all,
isn't ES a classic straw man hypothesis? How long will
EVOLUTIONARY PATTERN TERMINOLOGY
515
Table 1. Definitions for evolutionary effect terms introduced in the text
Evolutionary effect term
An evolutionary pattern in which. . .
Evolutionary inertia
. ..a character with an unchanged character state will remain unchanged
~
~~~
and a character experiencing consistent directional change will maintain
that evolutionary pattern between generations of a lineage unless an
external resultant force acts on it.
Evolutionary inertia (operational)
. . .a character with an unchanged character state will remain unchanged
and a character experiencing consistent directional change will maintain
that evolutionary pattern between branches of a phylogenetic tree unless
an external resultant force acts on it.
Evolutionary stasis
. ..a character has a static evolutionary inertial state.
Evolutionary thrust
. . . a character has an evolutionary inertial state of consistent directional
evolutionary change.
Evolutionary constraint
. . . a character fails to change in an adaptive manner due to preventative
factors or mechanisms.
Evolutionary momentum
...a character fails to change in an adaptive manner due to previous
evolutionary pathways.
Evolutionary acceleration
. . . a character shows increasing rates of evolutionary change in a
consistent direction.
a trait maintain stasis without alteration by mutation,
drift and selection? Coddington (1988: 18) addressed
this point: “The view that features may have been
adaptive a t some point, but are now maintained by
something other than selection, is probably the most
widely accepted explanation of synapomorphy among
biologists today. It is a weak theory which nevertheless
may be correct for the majority of features.” Felsenstein
(1985: 6) states ‘It may be doubted how often evolutionary inertia is effectively absent.” Evolutionary
stasis is what makes our field of study possible. Resistance to concepts of ES is primarily based on perceptions that traits for which adaptive evolutionary
patterns are studied should be plastic. These traits
are presumed readily malleable by available ecological
circumstances. However, recent studies have demonstrated that many of o u r assumptions about character malleability must be re-examined (de Queiroz
& Wimberger, 1993; Paterson, Wallis & Gray, 1995).
Evolutionary stasis is not a straw man hypothesis and
in many cases evolutionary biologists will be unable
to provide data to reject it.
Evolutionary stasis may seem to apply only to characters that lack polymorphism. However, consider a n
extreme case of polymorphism in which a polygenic
character shows continuous variation in a population
due to genetic polymorphism a t each locus. One might
assume that consistently applied evolutionary forces
such as stabilizing selection are needed for this distribution to remain unaltered between generations
(Maynard Smith et aZ.,1985). I argue that ES is still
the appropriate null model for this character. In this
case, we assume that each gene locus involved with
the trait is in Hardy-Weinberg equilibrium. This point
is crucial. Evolutionary stasis is simply HardyWeinberg equilibrium extrapolated to a different scale
of examination but with the same underlying assumptions. If Hardy-Weinberg is the appropriate null
model for population genetic and microevolutionary
studies then ES is the logical extension for macroevolutionary studies. Only with this beginning assumption can we recognize alternative evolutionary
patterns and how they relate to the processes of genetic
drift and selection.
It is tempting to assume that some constraints to
evolution are in place when a pattern of ES is seen.
However, to identify EC one must first demonstrate
why a specific evolutionary transition is expected and
identify the factors preventing this transition. In most
studies, even if ECs are occurring, they should be
described as ES until the identification of specific
constraining mechanisms is possible. Comparative
methods that attempt to ‘control for phylogeny’ cannot
identify the detailed patterns of lineages in stasis,
possibly due to constraints. Tree-thinking and understanding the evolution of constrained characters and
the constraining mechanisms are crucial for understanding EC (McKitrick, 1993).
Failure to reject a null hypothesis of ES does not
give us a greater understanding of evolution. However,
identification of EC, EM, ET, and EA patterns can
help us understand the operation of underlying evolu-
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D.B.BURT
tionary mechanisms. For example does release from
EC serve as a key innovation for rapid diversification
(McKitrick, 1993)? Do ECs commonly lead to convergent evolution of certain traits (Maynard Smith et
al., 1985; Wake, 1991)?How commonly andunder what
narrow circumstances do we see ET and EA? After
release from EC do traits show EA?
In some cases an overlapping use of terms will be
appropriate. The examples of sexual selection in this
paper used the terms ET, EC and EA to refer to the
same phenomenon. This overlap does not relate to any
defect in the definitions of these terms but instead
reflects the complexity of nature. Nature cannot always
be easily categorized. Each term defined here can
describe major evolutionary patterns in a logical manner and allow us to more effectively communicate o u r
interpretations of evolutionary patterns. I hope that
those who have judged evolutionary effects terms in
the past in a less than favourable manner will take a
second look a t their potential applicability.
ACKNOWLEDGEMENTS
I thank D. Maddison and W. Maddison for initially
forcing me to think deeply about the meaning of evolutionary inertia. K. Bostwick, M. Brady, K. Johnson, K.
Omland, and students in my graduate evolution course
a t SFA provided helpful comments during the initial
formation of ideas presented here. S. Burt, P. Coulter,
A. de Queiroz, M. Hedin and two anonymous reviewers
deserve special thanks for helpful comments on earlier
versions of the manuscript.
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