On the effect of asymmetrical trait inheritance on models of trait evolution

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.Funding provided by: Swiss National Science Foundation*Crossref Funder Registry ID: Award Number: 31003A-163428Funding provided by: Swedish Research Council*Crossref Funder Registry ID: Award Number: 2015-04748Funding provided by: Swiss National Science FoundationCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100001711Award Number: 31003A-163428Funding provided by: Swedish Research CouncilCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100004359Award Number: 2015-04748Data set generated through simulations by using the script PhyloTraitSimulator.