Evolvability in the fossil record

Abstract

The concept of evolvability—the capacity of a population to produce and maintain evolutionarily relevant variation—has become increasingly prominent in evolutionary biology. Paleontology has a long history of investigating questions of evolvability, but paleontological thinking has tended to neglect recent discussions, because many tools used in the current evolvability literature are challenging to apply to the fossil record. The fundamental difficulty is how to disentangle whether the causes of evolutionary patterns arise from variational properties of traits or lineages rather than being due to selection and ecological success. Despite these obstacles, the fossil record offers unique and growing sources of data that capture evolutionary patterns of sustained duration and significance otherwise inaccessible to evolutionary biologists. Additionally, there exist a variety of strategic possibilities for combining prominent neontological approaches to evolvability with those from paleontology. We illustrate three of these possibilities with quantitative genetics, evolutionary developmental biology, and phylogenetic models of macroevolution. In conclusion, we provide a methodological schema that focuses on the conceptualization, measurement, and testing of hypotheses to motivate and provide guidance for future empirical and theoretical studies of evolvability in the fossil record.

Evolvability and Macroevolution: Overview and Synthesis

“…As in many other aspects of macroevolution, contingency is a factor when considering the potential role of trait covariation in evolvability. If rate and net distance traversed in morphospace is the evolvability measure, as suggested here, the covariation structure imposed by morphological integration-as noted, not strictly the antithesis of modularity but useful in this context-can enable more rapid and extensive evolutionary change in certain directions than would emerge from strictly isotropic or unbiased variation (Felice et al, 2018;Goswami et al, 2014;Jablonski, 2020;Love et al, 2021;Uller et al, 2018). Thus, in the special circumstance when selection (i.e.…”

“…Thus, the utility of extrapolating from present-day data (Hansen & Pélabon, 2021), and their roles in determining properties such as modularity or the isotropy of accessible phenotypes around a given starting point, is debated, with a variety of empirical outcomes. Further analyses in a multispecies phylogenetic framework would be valuable (see Love et al, 2021;and Saltzberg et al, 2022, relatively narrow in its phenotypic and phylogenetic coverage but encouraging in not finding a correlation between G-matrix divergence and time since species splits). Urgently needed for such crossscale applications is an array of genetic and developmental model systems that have robust fossil records.…”

“…Here too some progress has been made, but separating speciation and extinction rates from net diversification-potentially important for testing hypotheses of cause and effect in morphospace occupation (as in Huang et al, 2015)-remains challenging (e.g. Louca & Pennell, 2020;Love et al, 2021), as does the problem of inferring ancestral character states from extant taxa alone (Betancur-R et al, 2015;Marshall, 2017;Slater et al, 2012); and as Mangiardino Koch (2021) notes more generally (citing twelve studies), evolutionary modeling is demonstrably improved and results shift when fossils are incorporated.…”

“…The general view has been that greater modularity enhances evolvability (e.g. Love et al, 2021;Vermeij, 1974Vermeij, , 2015versatility", which he associates with modularity in the later paper; Wagner & Altenberg, 1996). However, many different types of modules are recognized, i.e., functional, developmental, genetic, and evolutionary modules (references in Jablonski, 2017a), and we lack clarity on how they are related, with mixed results on the positive, negative, or negligible relation between the strength of modularity and macroevolution (Rhoda et al, 2021 and references therein).…”

“…(a) Speciation may tend to occur preferentially in the direction of intraspecific (co)variation (Hunt, 2007;Love et al, 2021;Polly & Mock, 2018), providing a potential link between standing variation and both developmental bias and macroevolutionary evolvability, with high-speciation clades moving more rapidly across morphospace per unit time, and more efficiently in that fewer species go in the opposing direction over the course of the trend-Gould's ( 1982) "direction bias" in clade dynamics (see also Jablonski, 2020). (Similar results are reported, mostly over shorter time scalesperhaps just a few generations-for patterns of genetic (co)variance and phenotypic divergences, but as noted above macroevolutionary predictions may be undermined by the complex, nonlinear relationships between genotype and phenotype often described as G-matrices and P-matrices (Hallgrímsson et al, 2022;Milocco & Salazar-Ciudad, 2022; but see Saltzberg et al, 2022 for a possible counter-example).…”