Evolutionary stasis, constraint and other terminology describing evolutionary patterns

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 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: 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 Department of Biology, Stephen l? Austin State University, PO. Box 13003, SFA Station, Nacogdoches, Texas 75962-3003, USA 510 D.B.BUW 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 impli (...truncated)