Evolvability and Macroevolution: Overview and Synthesis

Abstract

Evolvability is best addressed from a multi-level, macroevolutionary perspective through a comparative approach that tests for among-clade differences in phenotypic diversification in response to an opportunity, such as encountered after a mass extinction, entering a new adaptive zone, or entering a new geographic area. Analyzing the dynamics of clades under similar environmental conditions can (partially) factor out shared external drivers to recognize intrinsic differences in evolvability, aiming for a macroevolutionary analog of a common-garden experiment. Analyses will be most powerful when integrating neontological and paleontological data: determining differences among extant populations that can be hypothesized to generate large-scale, long-term contrasts in evolvability among clades; or observing large-scale differences among clade histories that can by hypothesized to reflect contrasts in genetics and development observed directly in extant populations. However, many comparative analyses can be informative on their own, as explored in this overview. Differences in clade-level evolvability can be visualized in diversity-disparity plots, which can quantify positive and negative departures of phenotypic productivity from stochastic expectations scaled to taxonomic diversification. Factors that evidently can promote evolvability include modularity—when selection aligns with modular structure or with morphological integration patterns; pronounced ontogenetic changes in morphology, as in allometry or multiphase life cycles; genome size; and a variety of evolutionary novelties, which can also be evaluated using macroevolutionary lags between the acquisition of a trait and phenotypic diversification, and dead-clade-walking patterns that may signal a loss of evolvability when extrinsic factors can be excluded. High speciation rates may indirectly foster phenotypic evolvability, and vice versa. Mechanisms are controversial, but clade evolvability may be higher in the Cambrian, and possibly early in the history of clades at other times; in the tropics; and, for marine organisms, in shallow-water disturbed habitats.

Cambrian origin but no early burst in functional disparity for Class Bivalvia

“…The onset of their Ordovician diversification coincided with an increase in nutrients and ocean ventilation [45] and the transformation of the seafloor from surfaces stabilized by microbial mats to softer, bioturbated sediments [15,29], with bivalves expanding into both on- and offshore habitats with soft- and hard-ground substrata [43]. Thus, bivalves may be another instance of a clade whose diversification required a chain of derived characters, rather than a single “key innovation” [46,47].…”

Aggregate Trait Evolvability and Macroevolution in Two Sister Species of the Bryozoan Stylopoma

“…We use evolvability, as defined by Houle (1992), to determine whether aggregate traits in colonies can evolve. Evolvability is a measure of trait variance that is scaled by the trait mean, and can be interpreted as the maximum possible rate of evolutionary change that can occur across a single generation under direct selection (Houle, 1992;Hansen & Houle, 2008;Love et al, 2021;Jablonski, 2022).…”

Temperature-Dependent Enhanced Speciation in Ecosystems with Conserved Symmetries

“…After all, there have been studies on the effect of temperature on rates of spontaneous mutation that could drive speciation (Husby et al, 2011;Waldvogel and Pfenninger, 2021;Z Lu et al, 2021;Gillman and Wright, 2014;Chu et al, 2018). What factors drive mutation and the divergence of species have been a recurring experimental and theoretical question (Jablonski, 2022;Livnat, 2017;Smith et al, 2014). In this paper, the effect of changing temperatures as it perturbs the balance in nature is investigated from an analytical framework.…”