Rates of Evolution in Developmental Processes

AMER. ZOOL., 32:123-134 (1992) Rates of Evolution in Developmental Processes1 GREGORY A. WRAY Friday Harbor Laboratories and Department of Zoology, University of Washington, 620 University Road, Friday Harbor, Washington 98250 in developmental processes. Such an endeavor would be interesting because From the outset, rates of change have formed a central theme in studies of mac- development plays a central role in evoluroevolution (Simpson, 1944, 1953; Hal- tion, mechanistically linking genomic and dane, 1949; Stanley, 1979). Evolutionary morphological change. It therefore seems rates remain an important component in likely that rates of change in developmental contemporary macroevolution, as attested process will provide insights into evoluby the interest generated by the punctuated tionary rate phenomena. For example, equilibrium debate and the growing atten- development can dissociate rates of genotion on rates of genomic change. Evolu- mic and phenotypic change by amplifying tionary rate studies have focused on differ- or buffering the effects of mutations. Of parences in rates of evolution between clades ticular interest is the possibility that rates and on uneven rates of evolution within of developmental evolution may constrain clades (Simpson, 1944; Stanley, 1979,1985). or boost rates of change in morphology. Differences in rates of evolution may influThis paper explores tempo and mode in ence clade diversity, shape, and persistence the evolution of development. I begin by by affecting speciation rates and the origin providing methods for reconstructing and of evolutionary innovations (Simpson, 1944; dating evolutionary transformations in Eldredge and Gould, 1972; Van Valen, 1974; development. Following this approach, it is Stanley, 1979). possible to estimate minimum average rates Historically, most evolutionary rate stud- of evolution in quantitative developmental ies have focused on change in adult mor- parameters, as well as the duration that phology, although increasing attention is complex qualitative transformations in now being directed towards rates of molec- developmental processes take to evolve. ular evolution. To date, however, no attempt Using these methods I then demonstrate that has been made to assess rates of evolution development processes can evolve at rates comparable to adult morphology, and that rates of evolution in development can vary 1 From the Symposium on Development and Macby over two orders of magnitude within a roevolution sponsored by the Division of the History clade. Finally, I consider the relevance of and Philosophy of Biology of the American Society of variable rates of change in developmental Zoologists and presented at the Annual Meeting of the processes to macroevolution, including the American Society of Zoologists, 27-30 December 1990, at San Antonio, Texas. decoupling of genomic and morphological INTRODUCTION 123 SYNOPSIS. The tempo and mode of morphological evolution are influenced by several factors, among which evolutionary transformations in developmental processes are likely to be important. Comparing the embryos of extant species in an explicit phylogenetic framework allows the estimation of minimum average rates of evolution in quantitative developmental parameters. It also allows delineation of the maximum time that complex qualitative transformations in developmental mechanism take to evolve. This paper analyzes rates of quantitative and qualitative developmental evolution using examples drawn primarily from echinoderms. The results demonstrate that rates of developmental evolution can be comparable to rates of morphological evolution. There is no indication that rates of evolution in development are lower for earlier stages, contrary to the prediction of "tree" models of epigenetic interactions. In particular, rates of evolution in oogenesis can exceed rates of evolution in adult body size. Rates of developmental evolution can vary by up to two orders of magnitude within a clade. Whether such large scale variation in evolutionary rates of developmental processes is a general phenomenon can only be answered by further study. 124 GREGORY A. WRAY rates of change, the possibility of stage-specific rates of developmental evolution, and the extent to which developmental processes may limit evolutionary changes in body plans. RECONSTRUCTING THE EMBRYOS OF ANCESTORS MEASURING RATES OF EVOLUTION IN DEVELOPMENT Evolutionary changes in development take many forms and affect a wide variety of processes. As explained below, however, it is only necessary to distinguish between quantitative and qualitative transformations when estimating rates of evolution in developmental processes. Because modifications can evolve in developmental processes without significantly affecting adult morphology (Elinson, 1987; Strathmann, 1988a; Raff et ai, 1991), rates of morphological evolution in adults can underestimate rates of evolution in development. Estimating evolutionary rates in quantitative parameters Much about development is inherently quantitative, including parameters of size, rate, and time. Quantitative change, particularly in the form of heterochrony, is a common component in the evolution of development (McNamara, 1988; Raff and Wray, 1989). For the purposes of comparison between taxa, it is preferable to calculate proportional, rather than absolute, rates of evolution in quantitative features (Haldane, 1949; Simpson, 1953; Van Valen, 1974). The minimum average proportional rate of evolution, r, in a quantitative parameter, P, is: _ _ 1 dV _ ln(P de J - ln(Panc) r "PdT i (1) where Panc and Pdesc are the values of the parameter in an ancestor and a descendant, and where t is the elapsed time (Haldane, 1949). Although the embryos of extinct ancestors cannot be studied directly, there is much that can be learned about them from their living descendants. An analysis of character evolution (Maddison et ai, 1984; Swofford and Maddison, 1987; Donoghue, 1989) provides a means of reconstructing ancestral ontogenies: differences in the developmental processes of extant species are mapped onto an independently derived phylogeny, and ancestral states at each node are inferred using biologically reasonable parsimony assumptions. As with variation in any other trait, outgroups can be used to polarize character state transformations (Farris, 1982; Swofford and Maddison, 1987). When combined with estimated divergence times, this type of analysis can be used to date specific evolutionary transformations in development (Wray and Raff, 1991a). As an example, consider the evolution of, developmental processes within the echinoderm class Echinoidea (sea urchins, sand dollars, and their kin). Features of early echinoid development such as radial, holoblastic cleavage, and regulative early cell divisions are symplesiomorphies for the phylum Echinodermata; they are present in extant echinoids and were almost certainly present (...truncated)