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The Continuity of Microevolution and Macroevolution

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The Continuity of Microevolution and Macroevolution The continuity of microevolution and macroevolution ANDREW M. SIMONS Department of Biology, College of Natural Sciences, Carleton University, Ottawa, Ont., Canada Keywords: Abstract adaptation; A persistent debate in evolutionary biology is one over the continuity of bet-hedging strategy; microevolution and macroevolution – whether macroevolutionary trends are environmental variance; governed by the principles of microevolution. The opposition of evolutionary evolutionary constraint; trends over different time scales is taken as evidence that selection is geometric-mean fitness; uncoupled over these scales. I argue that the paradox inferred by trend macroevolution; opposition is eliminated by a hierarchical application of the Ôgeometric-mean mass extinction; fitnessÕ principle, a principle that has been invoked only within the limited microevolution; context of microevolution in response to environmental variance. This natural selection; principle implies the elimination of well adapted genotypes – even those with optimality. the highest arithmetic mean fitness over a shorter time scale. Contingent on premises concerning the temporal structure of environmental variance, selectivity of extinction, and clade-level heritability, the evolutionary outcome of major environmental change may be viewed as identical in principle to the outcome of minor environmental fluctuations over the short-term. Trend reversals are thus recognized as a fundamental property of selection operating at any phylogenetic level that occur in response to event severities of any magnitude over all time scales. This Ôbet-hedgingÕ perspective differs from others in that a specified, single hierarchical selective process is proposed to explain observed hierarchical patterns of extinction. to oppose trends occurring between these events. A Introduction pattern of self-similarity of extinction at different tem- The continuity of selective processes over microevolu- poral scales has been observed (Raup, 1986; Sole´ et al., tionary and macroevolutionary time continues to be a 1997; McKinney & Frederick, 1999; Plotnick & Sepkoski, source of disagreement in evolutionary biology (Sole´ 2001), fuelling further discussion of evolutionary et al., 1999; Erwin, 2000; Carroll, 2001; Plotnick & mechanisms – beyond principles of microevolution – Sepkoski, 2001), one that Maynard Smith (1989) driving trends at different time scales (Sole´ et al., 1999; described as Ôunsatisfactory.Õ In dispute is whether the Plotnick & Sepkoski, 2001). This is a debate, then, about effects of selection operating over microevolutionary the relevance of the process of natural selection operating time, or at the population level, account for observed at the Ôecological momentÕ (Gould, 1985) to the produc- trends over macroevolutionary time. That any particular tion of phenotypic trends over the long-term. evolutionary event can be explained by the neo-Dar- Resolution of the continuity issue is critical because if winian synthetic theory (Charlesworth et al., 1982) does selection is discontinuous over different time scales, then not imply that the evolutionary consequences of rare palaeobiology and evolutionary genetics are not two events such as mass and minor extinctions will not tend approaches to the same evolutionary problems; they are only distantly related fields of study. Furthermore, disagreement over the relative importance of natural Correspondence: Andrew M. Simons, Department of Biology, College of selection in determining trends over different time scales Natural Sciences, Carleton University, 1125 Colonel By Drive, Ottawa, Ont., Canada K1S 5B6. is eagerly distorted by anti-evolutionist groups to Tel.: 613-520-2600; ext. 3869; fax: 613-520-3539; discredit both macroevolution as lacking a mechanism, e-mail: [email protected] and microevolution as being restricted to insignificant 688 J. EVOL. BIOL. 15 (2002) 688–701 ª 2002 BLACKWELL SCIENCE LTD Microevolution and macroevolution 689 phenotypic change. The fact that the debate has not been example, Jablonski (1997) argues that, whereas body resolved means that a single perspective of selection size is an important fitness correlate in microevolution, consistent with both micro- and macroevolution is still Cope’s rule – a trend of increasing body size through time needed. In this paper, I propose that no new theory is – plays a Ôweak or unpredictable roleÕ in macroevolution. needed to attain this perspective; rather, it is attained To explain such contrasting trends, a qualitative differ- through the broad application of an existing theory with ence between processes operating during the mass a previously underappreciated significance. extinctions and during background times is proposed Before making the argument for the continuous nature (Jablonski, 1986). Under this view, mass extinctions are of selection, the rationale for views of discontinuity of not caused merely by an intensification of background selection operating over different time scales will be selection: an alternation of macroevolutionary regimes considered. The remainder of the paper presents a case would explain opposing trends in survival, and survival for the applicability of the principles of bet-hedging over the longer term would depend on the Ôchance theory, which are conventionally restricted to excep- occurrenceÕ of traits allowing survival under both regimes tional circumstances, to evolution in general. The rele- (Jablonski, 1986). vance of the perspective will depend on premises about Raup (1986) sees mass extinctions as one extreme on the interaction among patterns of environmental vari- the continuum of environmental variance, but envisions ance over different time scales, selectivity imposed by this a dichotomy between ÔdestructiveÕ and ÔconstructiveÕ environmental variance, and the heritability or phylo- forces operating over different time scales. He argues genetic nesting of traits. Support for the premises is found that, in order to be constructive, an environmental event in the literature and provides reason to accept the must occur often enough to be within the ÔexperienceÕ of argument in principle. The paper concludes with exam- the organism (Raup, 1986); hence, extinction is a ples illustrating how the integration of bet-hedging ideas nonconstructive evolutionary force (Raup, 1986). Simi- into evolutionary theory results in a self-consistent view larly, in a theory to account for evolution above the of the way in which natural selection operates. species level, Stanley (1975) proposes that higher level processes are necessary to explain evolutionary trends, Views of discontinuity and that natural selection provides Ôlittle more than the raw material and fine adjustment of large-scale evolu- The existence of the terms ÔmicroevolutionÕ and Ômacro- tionÕ (Stanley, 1975). evolutionÕ reflects the controversy (Eldredge & Gould, Rather than an alternation between two processes, 1972; Stanley, 1975; Orzack, 1981; Charlesworth et al., Gould (1985) proposes a three-tiered model of evolution 1982; Maynard Smith, 1989; Gould & Eldredge, 1993; to account for the ÔparadoxÕ implied by the uncorrelated Van Valen, 1994; Bennett, 1997; Erwin, 2000; Carroll, evolutionary trends across time scales. Evolution at the 2001) over the unity of the process of natural selection three tiers (ecological moments, normal geological time, operating at different time scales. Gould (1985), for and periodic mass extinctions) is governed by distinct example, contends that the process of selection is of a processes with independent Ôrules and principlesÕ (Gould, different nature at different time scales. His argument is 1985). Gould (1985) asserts ÔWe will all, I trust, at least based on the observation that what is seemingly an allow that creatures cannot prepare for catastrophes of adaptive trend over one time scale is not consistent with such spacing and that their adaptive struggles at the first trends over another. For this reason, Gould stated that tier can therefore, at the very best, only produce the synthetic theory, at least as portrayed by Mayr, is exaptations for later debacles.Õ Thus, for Gould (1985), Ôeffectively deadÕ (Gould, 1980; but see Gould, 1985); trends over normal geological time are autonomous, and adaptation over a few generations is insignificant because the accumulation of adaptations occurring at the first tier major evolutionary trends are not established by proces- are Ôreversed, undone, and overriddenÕ. Bennett (1997), ses circumscribed by the modern synthesis (Gould, with the intention of Ôlinking evolution with ecologyÕ 1985). Even if population genetic theory can explain which, in his view had been decoupled by Darwin, adds a patterns observed in the fossil record (Charlesworth et al., fourth tier to Gould’s three. He envisions different 1982), it does not address the problem of why the fossil processes acting concurrently over four time scales to record should reveal trends contrary to those observed account for observed trends within each, and calls this over microevolutionary time. Implicit in the disagree- view the Ôpostmodern evolutionary synthesisÕ (Bennett, ment is that the outcome of selection is qualitatively 1997, p. 184). Bennett outlines the relevance of individ- different when acting at different levels, but the rela- ual lifespans to his arguments (Bennett, 1997, p. 176): tionship between these outcomes has remained indis- diurnal and seasonal changes, unlike fluctuations over tinct. longer time scales, are predictable and thus may form an
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