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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 I DE c3 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 * E-mail: [email protected] 0024-4066/01/040509 + 09 $35.00/0 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 & 509 0 2001 The Linnean Society of London 510 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 511 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 512 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 513 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: 514 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- 516 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. REFERENCES Anderson DJ, Stoyan NC, Ricklefs RE. 1987. Why are there no viviparous birds? A comment. American Naturalist 130: 941-947. Antonovics J, van Tienderen PH. 1991. Ontoecogenophyloconstraints? The chaos of constraint terminology. 72Pnds in Ecology & Evolution 6 166-168. Baum DA, Larson A. 1991. Adaptation reviewed A phylogenetic methodology for studying character macroevolution. Systematic Zoology 4 0 1-18. Berger J. 1988. Social systems, resources, and phylogenetic inertia: an experimental test and its limitations. In: Slobodchikoff CN, ed. The ecology of social behavior. San Diego: Academic Press, 157-186. Blackburn DG, Evans HE. 1986. Why are there no viviparous birds? American Naturalist 128 165-190. Brooks DR, McLennan DA. 1991. Phylogeny, Ecology, and Behavior Chicago: University of Chicago Press. Cheverud JM, Dow MM, Leutenegger W. 1985. The quantitative assessment of phylogenetic constraints in comparative analyses: Sexual dimorphism in body weight among primates. Evolution 3 9 1335-1351. Coddington JA. 1988. Cladistic tests of adaptational hypotheses. Cladistics 4 3-22. de Queiroz A, Wimberger P. 1993. The usefulness of behavior for phylogeny estimation: Levels of homoplasy in behavioral and morphological characters. Evolution 47: 46-60. Derrickson EM, Ricklefs RE. 1988. Taxon-dependent diversification of life-history traits and the perception of phylogenetic constraints. Functional Ecology 2 417423. Diniz-Filho JAF’, de Sant’Ana CER, Bini LM. 1998. An eigenvector method for estimating phylogenetic inertia. Evolution 5 2 1247-1262. Edwards SV, Naeem S. 1993. The phylogenetic component of cooperative breeding in perching birds. American Naturalist 141: 754-789. Felsenstein J. 1985. Phylogenies and the comparative method. American Naturalist 125 1-15. Gould SJ,Lewontin RC. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London Series B Biological Sciences 205: 581-598. Harvey PH, Page1 MD. 1991. The comparative method in evolutionary biology. Oxford: Oxford University Press. Harvey P, Purvis A. 1991. Comparative methods for explaining adaptations. Nature 351: 61W324. Jamieson IG. 1989. Behavioral heterochrony and the evolution of birds’ helping a t the nest: an unselected consequence of communal breeding? American Naturalist 133 394406. Janzen DH, Martin PS. 1982. Neotropical anachronisms: The fruits the gomphotheres ate. Science 215 19-27. Kusmierski R, Borgia G, Uy A, Crozier RH. 1997. Labile evolution of display traits in bowerbirds indicate reduced effects of phylogenetic constraint. Proceedings of the Royal Society of London Series B 264: 307-313. Leroi AM, Rose MR, Lauder GV. 1994. What does the comparative method reveal about adaptation? American Naturalist 143 381402. Ligon JD. 1993. The role of phylogenetic history in the evolution of contemporary avian mating and parental care systems. Current Ornithology 10: 1 4 6 . Maddison WP. 1990. A method for testing the correlated evolution of two binary characters: are gains or losses concentrated on certain branches of a phylogenetic tree? Evolution 44:539-557. Maddison W, Slatkin M. 1991. Null models for the number of evolutionary steps in a character on a phylogenetic tree. Evolution 45: 1184-1197. Maddison W, Maddison DR. 1992. MacClade: Analysis of Phylogeny and Character Evolution. Sunderland, Massachusetts: Sinauer Associates. Maynard Smith J, Burian R, Kauffman S, Alberch P, Campbell J, Goodwin B, Lande R, Raup D, Wolpert L. 1985. Developmental constraints and evolution. Quarterly Review of Biology 60: 265-287. McKitrick MC. 1993. Phylogenetic constraint in evolutionary theory: has it any explanatory power? Annual Review of Ecology and Systematics 24: 307-330. McLain DK. 1993. Cope’s rules, sexual selection, and the loss of ecological plasticity. Oikos 68: 490-500. EVOLUTIONARY PA!lTERN TERMINOLOGY Nakatsukasa M. 1996. Locomotor differentiation and different skeletal morphologies in mangabeys (Lophocebus and Cercocebus).Folia Primatologica 66:15-24. Paterson AM, Wallis GP, Gray RD. 1995. Penguins, petrels, and parsimony: does cladistic analysis of behavior reflect seabird phylogeny. Evolution 4 9 974-989. Peterson AT, Burt DB. 1992. Phylogenetic history of social evolution and habitat use in the Aphelocoma jays. Animal Behaviour 44:859-866. Prum RO. 1994. Phylogenetic analysis of the evolution of alternative social behavior in the manakins (Aves: Pipridae). Evolution 48.1657-1675. Ridley M. 1983. The explanation of organic diversity: The comparative method and adaptations for mating. Oxford Clarendon Press. Riedl R. 1978. O&r in living ozanisms. New York: John Wiley & Sons. Schluter D, Price T, Mooers A0, Ludwig D. 1997. Like- 517 lihood of ancestral states in adaptive radiation. Evolution 51: 1699-1711. Schwenk K. 1995. Of tongues and noses: chemoreception in lizards and snakes. Trends in Ecology & Evolution 1 0 7-12. Serway RA, Faughn JS. 1985. College physics. Philadelphia: Saunders College Publishing. Wagner PJ. 1995. Testing evolutionary constraint hypotheses with early Paleozoic gastropods. Paleobiology 21: 248-272. Wake DB. 1991. Homoplasy: the result of natural selection, or evidence of design limitations? American Naturalist 138: 543-567. Winkler DW, Sheldon FH. 1993. Evolution of nest construction in swallows (Hirundinidae): A molecular phylogenetic perspective. Pmeedings of the National Academy of Sciences, USA 90:5705-5707.