On the Effect of Asymmetrical Trait Inheritance on Models of Trait Evolution

Abstract

Current phylogenetic comparative methods modelling quantitative trait evolution generally assume that, during speciation, phenotypes are inherited identically between the two daughter species. This, however, neglects the fact that species consist of a set of individuals, each bearing its own trait value. Indeed, because descendent populations after speciation are samples of a parent population, we can expect their mean phenotypes to randomly differ from one another potentially generating a “jump” of mean phenotypes due to asymmetrical trait inheritance at cladogenesis. Here, we aim to clarify the effect of asymmetrical trait inheritance at speciation on macroevolutionary analyses, focusing on model testing and parameter estimation using some of the most common models of quantitative trait evolution. We developed an individual-based simulation framework in which the evolution of species phenotypes is determined by trait changes at the individual level accumulating across generations and cladogenesis occurs then by separation of subsets of the individuals into new lineages. Through simulations, we assess the magnitude of phenotypic jumps at cladogenesis under different modes of trait inheritance at speciation. We show that even small jumps can strongly alter both the results of model selection and parameter estimations, potentially affecting the biological interpretation of the estimated mode of evolution of a trait. Our results call for caution when interpreting analyses of trait evolution, while highlighting the importance of testing a wide range of alternative models. In the light of our findings, we propose that future methodological advances in comparative methods should more explicitly model the intra-specific variability around species mean phenotypes and how it is inherited at speciation.

Extinction and the temporal distribution of macroevolutionary bursts

“…Our study complements this view, but with an important distinction: our models do not invoke speciation and only permit anagenetic change. Although the Ephemeral Speciation model (and other models of speciation‐dependent trait evolution; Duchen et al., 2020) emphasizes divergence that was aborted, our models emphasize the importance of extinction for the divergence that cannot accrue in the first place, representing simply one example of the general challenge that extinction imposes for comparative biology. As our ability to infer microevolutionary fitness surface is limited to the distribution of phenotypes we observe, our understanding of the shape and dynamics of macroevolutionary adaptive landscapes is limited by a reliance upon those lineages that have not gone extinct.…”

Métodos de reconstrucción filogenética I: máxima verosimilitud

“…Dada la relevancia biológica de conocer las relaciones evolutivas entre distintas especies, inferir una filogenia a partir de datos morfológicos o moleculares es una práctica muy efectuada en biología evolutiva y taxonomía. Por otro lado, las filogenias también se usan para reconstruir caracteres ancestrales (Pagel, 1999), establecer relojes moleculares (Bronham & Penny, 2003), o para estudiar la evolución de caracteres morfológicos (Duchen, Alfaro, Rolland, Salamin & Silvestro, 2020).…”

A multi‐platform package for the analysis of intra‐ and interspecific trait evolution

“…Instead, they often consider intraspecific variation as a variance-introducing factor to be dealt with by an error term (but see, Felsenstein, 2008;Ives, Midford, & Garland, 2007;Mendes, Fuentes-González, Schraiber, & Hahn, 2018;Revell & Graham Reynolds, 2012;Silvestro, Kostikova, Litsios, Pearman, & Salamin, 2015). Intraspecific variation is nonetheless not merely a nuisance parameter, but a key evolutionary component (Duchen, Alfaro, Rolland, Salamin, & Silvestro, 2019). Many factors have been shown to affect the evolution of intraspecific variation, which in turn has an influence on the driving forces of species evolution and diversification (Darwin, 1859;MacArthur, 1965).…”