Approaches to Macroevolution: 1. General Concepts and Origin of Variation

Abstract

Approaches to macroevolution require integration of its two fundamental components, i.e. the origin and the sorting of variation, in a hierarchical framework. Macroevolution occurs in multiple currencies that are only loosely correlated, notably taxonomic diversity, morphological disparity, and functional variety. The origin of variation within this conceptual framework is increasingly understood in developmental terms, with the semi-hierarchical structure of gene regulatory networks (GRNs, used here in a broad sense incorporating not just the genetic circuitry per se but the factors controlling the timing and location of gene expression and repression), the non-linear relation between magnitude of genetic change and the phenotypic results, the evolutionary potential of co-opting existing GRNs, and developmental responsiveness to nongenetic signals (i.e. epigenetics and plasticity), all requiring modification of standard microevolutionary models, and rendering difficult any simple definition of evolutionary novelty. The developmental factors underlying macroevolution create anisotropic probabilities—i.e., an uneven density distribution—of evolutionary change around any given phenotypic starting point, and the potential for coordinated changes among traits that can accommodate change via epigenetic mechanisms. From this standpoint, “punctuated equilibrium” and “phyletic gradualism” simply represent two cells in a matrix of evolutionary models of phenotypic change, and the origin of trends and evolutionary novelty are not simply functions of ecological opportunity. Over long timescales, contingency becomes especially important, and can be viewed in terms of macroevolutionary lags (the temporal separation between the origin of a trait or clade and subsequent diversification); such lags can arise by several mechanisms: as geological or phylogenetic artifacts, or when diversifications require synergistic interactions among traits, or between traits and external events. The temporal and spatial patterns of the origins of evolutionary novelties are a challenge to macroevolutionary theory; individual events can be described retrospectively, but a general model relating development, genetics, and ecology is needed. An accompanying paper (Jablonski in Evol Biol 2017) reviews diversity dynamics and the sorting of variation, with some general conclusions.

Hierarchy in adaptive radiation: A case study using the Carnivora (Mammalia)

“…(Valentine , ; Jablonski and Bottjer ; Jablonski ; Erwin , ). By defining adaptive radiations in terms of their expected outcomes, rather than by the factors that promote them, empirical studies provide a direct route to the identification of traits associated with explosive ecological and morphological diversification, and the potential to answer critical questions about the relative importance of ecospace, morphological novelty, and developmental flexibility in promoting it (Erwin ; Jablonski ). As result, the critical question facing comparative evolutionary biologists is, we argue, not whether early burst adaptive radiation occurs but, rather, at what phylogenetic levels and in which niche traits it is most common.…”

Developmental bias in the fossil record

“…Due to the internal architecture of developmental systems, which generates integrated modules (Goswami, Binder, Meachen, & O'Keefe, 2015;Schlichting, 1989;Wagner & Zhang, 2011), random genetic mutations may still lead to coordinated phenotypic responses (Jablonski, 2017;Moczek et al, 2011;Uller et al, 2018;West-Eberhard, 2003). For this reason, the effects of the previously cryptic genetic variation may, in fact, cause directed phenotypic change, biased towards functionally integrated phenotypes (Gerhart & Kirschner, 2007;Masel, 2006;Wagner, 2011;Watson & Szathmáry, 2016;Watson, Wagner, Pavlicev, Weinreich, & Mills, 2014).…”

Developmental bias, macroevolution, and the fossil record

“…It is often treated as the converse of integration, although some care is needed in that an organism can have weak integration but lack discrete modules. P. Wagner et al, 2007;Espinosa-Soto & Wagner, 2010;Jablonski, 2017a;Larouche, Zelditch, & Cloutier, 2018). Weakening of integration and/or strengthening of modularity should thus tend to reduce the anisotropy of developmental bias by allowing evolution to occur in more directions, by promoting rate differentials among traits and modules, and perhaps by facilitating cooption of regulatory networks to build novel structures (Raff, 1996;G.…”

“…Biodiversity in all its dimensions or currencies cannot be understood without integrating the generation of raw material with its subsequent sorting (Gould, 2002;Jablonski, 2007Jablonski, , 2017a. One serious shortcoming of many recent treatments of the "extended synthesis" has been the neglect or omission of clade dynamics, that is the multilevel processes in sorting variation at, above, and below, the species level, and their effects at different temporal and spatial scales.…”