Can spatial sorting associated with spawning migration explain evolution of body size and vertebral number in Anguilla eels?

Anders Forsman,Hanna Berggren

doi:10.1002/ece3.2671

Abstract

Spatial sorting is a process that can contribute to microevolutionary change by assembling phenotypes through space, owing to nonrandom dispersal. Here we first build upon and develop the “neutral” version of the spatial sorting hypothesis by arguing that in systems that are not characterized by repeated range expansions, the evolutionary effects of variation in dispersal capacity and assortative mating might not be independent of but interact with natural selection. In addition to generating assortative mating, variation in dispersal capacity together with spatial and temporal variation in quality of spawning area is likely to influence both reproductive success and survival of spawning migrating individuals, and this will contribute to the evolution of dispersal‐enhancing traits. Next, we use a comparative approach to examine whether differences in spawning migration distance among 18 species of freshwater Anguilla eels have evolved in tandem with two dispersal‐favoring traits. In our analyses, we use information on spawning migration distance, body length, and vertebral number that was obtained from the literature, and a published whole mitochondrial DNA‐based phylogeny. Results from comparative analysis of independent contrasts showed that macroevolutionary shifts in body length throughout the phylogeny have been associated with concomitant shifts in spawning migration. Shifts in migration distance were not associated with shifts in number of vertebrae. These findings are consistent with the hypothesis that spatial sorting has contributed to the evolution of more elongated bodies in species with longer spawning migration distances, or resulted in evolution of longer migration distances in species with larger body size. This novel demonstration is important in that it expands the list of ecological settings and hierarchical levels of biological organization for which the spatial sorting hypothesis seems to have predictive power.

Highlights

The proposition (Lomolino, 1984; Shine et al, 2011) that evolutionary change might be driven by spatial sorting in the form of phenotype- and habitat-dependent dispersal capacity is interesting in this context
In its “neutral” form, cumulative spatial sorting and the resulting assortative mating process can potentially drive the evolution of more dispersive phenotypes even if variation in the dispersal-enhancing traits is not associated with lifetime reproductive success, that is in the absence of traditional natural selection (Phillips et al, 2006; Shine et al, 2011)
We take advantage of a phylogenetic hypothesis for Anguilla species (Minegishi et al, 2005) and use a comparative approach based on analysis of phylogenetic independent contrasts (Felsenstein, 1985; Purvis & Rambaut, 1995) to evaluate whether evolutionary shifts in spawning migration distance have been accompanied by evolutionary shifts in body size or in VN

Summary

| INTRODUCTION

In its “neutral” form, cumulative spatial sorting and the resulting assortative mating process can potentially drive the evolution of more dispersive phenotypes even if variation in the dispersal-enhancing traits is not associated with lifetime reproductive success, that is in the absence of traditional natural selection (Phillips et al, 2006; Shine et al, 2011). The potential for temporal assortative mating to drive directional evolutionary change increases if the quality of the spawning area declines over time, as in the case of the European eel (Righton et al, 2016; Figure 2b) These proposed scenarios should have resulted in the evolution of longer bodies and larger vertebral numbers in species of eels having longer spawning migration distances. We take advantage of a phylogenetic hypothesis for Anguilla species (Minegishi et al, 2005) and use a comparative approach based on analysis of phylogenetic independent contrasts (Felsenstein, 1985; Purvis & Rambaut, 1995) to evaluate whether evolutionary shifts in spawning migration distance have been accompanied by evolutionary shifts in body size or in VN

| MATERIALS AND METHODS

Findings

| DISCUSSION

| SUMMARY AND CONCLUSIONS