Extinction and the temporal distribution of macroevolutionary bursts.

Stephen P De Lisle,Locke Rowe,Njal Rollinson,David Punzalan

doi:10.1111/jeb.13741

Stephen P De Lisle, Locke Rowe + Show 2 more

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https://doi.org/10.1111/jeb.13741

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Abstract

Phenotypic evolution through deep time is slower than expected from microevolutionary rates. This is the paradox of stasis. Previous models suggest stasis occurs because populations track adaptive peaks that remain relatively stable on million‐year intervals, raising the equally perplexing question of why these large changes are so rare. Here, we consider the possibility that peaks can move more rapidly than populations can adapt, resulting in extinction. We model peak movement with explicit population dynamics, parameterized with published microevolutionary estimates. Allowing extinction greatly increases the parameter space of peak movements that yield the appearance of stasis observed in real data through deep time. Extreme peak displacements, regardless of their frequency, will rarely result in an equivalent degree of trait evolution because of extinction. Thus, larger peak displacements will rarely be inferred using trait data from extant species or observed in fossil records. Our work highlights population ecology as an important contributor to macroevolutionary dynamics, presenting an alternative perspective on the paradox of stasis, where apparent constraint on phenotypic evolution in deep time reflects our restricted view of the subset of earth's lineages that were fortunate enough to reside on relatively stable peaks.

Highlights

Phenotypic change can be rapid at microevolutionary timescales (Hendry & Kinnison1999; Kinnison & Hendry 2001; Gotanda et al 2015), consistent with strong selection (Endler 1987; Conner 2001) and abundant genetic variance (Mousseau & Roff 1987).Yet, analyses of microevolutionary, fossil, and comparative data on body size reveal that divergence is unexpectedly modest on slightly longer timescales, with cumulative divergence becoming substantial only over macroevolutionary time (Estes & Arnold2007; Uyeda et al 2011)
We show that in the presence of rapidly moving optima, populations may face extinction while attempting to track their adaptive peak, preventing these rapid peak shifts from being recorded as phenotypic change
Our work suggests that the observation of morphological stasis over macroevolutionary time may not reflect a lack of movement in phenotypic optima, but instead reflect our censored view of phenotypic evolution, which is restricted to those lineages that have not gone extinct

Summary

Introduction

Phenotypic change can be rapid at microevolutionary timescales (Hendry & Kinnison1999; Kinnison & Hendry 2001; Gotanda et al 2015), consistent with strong selection (Endler 1987; Conner 2001) and abundant genetic variance (Mousseau & Roff 1987).Yet, analyses of microevolutionary, fossil, and comparative data on body size reveal that divergence is unexpectedly modest on slightly longer timescales, with cumulative divergence becoming substantial only over macroevolutionary time (Estes & Arnold2007; Uyeda et al 2011). The pattern of limited phenotypic change over long timescales followed by macroevolutionary bursts suggests that some process must constrain phenotypic change within populations, as well as among closely related populations These results suggest that selection in the wild is net stabilizing, with shifts in the optimum phenotype occurring with exceptional rarity. Rather than solve the paradox of macroevolutionary stasis, these new results instead highlight two fundamental challenges in reconciling micro and macroevolution: 1) if peak shifts are rare, as suggested by analysis of phenotypic data, do we see similar patterns of peak shifts in microevolutionary studies of selection in the wild, and 2) what processes may account for discrepancies in our inference of evolutionary dynamics across short and deep time?

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