Abstract

Divergence in phenotypic traits is facilitated by a combination of natural selection, phenotypic plasticity, gene flow, and genetic drift, whereby the role of drift is expected to be particularly important in small and isolated populations. Separating the components of phenotypic divergence is notoriously difficult, particularly for multivariate phenotypes. Here, we assessed phenotypic divergence of threespine stickleback (Gasterosteus aculeatus) across 19 semi‐interconnected ponds within a small geographic region (~7.5 km2) using comparisons of multivariate phenotypic divergence (PST), neutral genetic (FST), and environmental (EST) variation. We found phenotypic divergence across the ponds in a suite of functionally relevant phenotypic traits, including feeding, defense, and swimming traits, and body shape (geometric morphometric). Comparisons of PSTs with FSTs suggest that phenotypic divergence is predominantly driven by neutral processes or stabilizing selection, whereas phenotypic divergence in defensive traits is in accordance with divergent selection. Comparisons of population pairwise PSTs with ESTs suggest that phenotypic divergence in swimming traits is correlated with prey availability, whereas there were no clear associations between phenotypic divergence and environmental difference in the other phenotypic groups. Overall, our results suggest that phenotypic divergence of these small populations at small geographic scales is largely driven by neutral processes (gene flow, drift), although environmental determinants (natural selection or phenotypic plasticity) may play a role.

Highlights

  • Phenotypic variation of natural populations results from a com‐ bination of evolutionary processes, gene flow, drift, natural selection, and environmentally induced phenotypic plas‐ ticity (Endler, 1986)

  • There were no clear difference between phenotypic diver‐ gence and neutral genetic differentiation for swimming traits, feed‐ ing traits, or body shape, suggesting that divergence in these traits may be mostly influenced by genetic drift or stabilizing selection

  • Our results suggest that phenotypic divergence in these small populations is driven by a combination of neutral processes and either natural selection or phenotypic plasticity in response to small‐scale environ‐ mental variation

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Summary

| INTRODUCTION

Phenotypic variation of natural populations results from a com‐ bination of evolutionary processes, gene flow, drift, natural selection, and environmentally induced phenotypic plas‐ ticity (Endler, 1986). One way to assess the relative contribution of natural selection and neutral processes (i.e., gene flow and drift) on phenotypic vari‐ ation, within and among natural populations, is to compare quan‐ titative trait (QST) and neutral genetic (FST) variation (Leinonen, McCairns, O'Hara, & Merilä, 2013). Comparing popula‐ tion pairwise QST and FST estimates in relation to population pair‐ wise estimates of ecological variation (EST) allows insight into the relative roles of divergent natural selection and neutral processes (selection vs gene flow vs drift) influencing phenotypic variation within and among populations (Hangartner, Laurila, & Räsänen, 2012; Kaeuffer, Peichel, Bolnick, & Hendry, 2012). Estimates of effective population size (Ne) further indicate that threespine stickleback populations in this area are generally small (Seymour et al, 2013, see below), making this system well‐suited to investigate the relative role of environmental selection/plasticity, gene flow, and drift in phenotypic divergence across small spatial scales.

| METHODS
| DISCUSSION
Findings
| CONCLUSIONS
CONFLICT OF INTERESTS
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