Evidence for contemporary and historical gene flow between guppy populations in different watersheds, with a test for associations with adaptive traits.

Léa Blondel,Ian Paterson,Lyndsey Baillie,Andrew P Hendry,Paul Bentzen,Jessica Quinton,Jahson B Alemu

doi:10.1002/ece3.5033

Abstract

In dendritic river systems, gene flow is expected to occur primarily within watersheds. Yet, rare cross‐watershed transfers can also occur, whether mediated by (often historical) geological events or (often contemporary) human activities. We explored these events and their potential evolutionary consequences by analyzing patterns of neutral genetic variation (microsatellites) and adaptive phenotypic variation (male color) in wild guppies (Poecilia reticulata) distributed across two watersheds in northern Trinidad. We found the expected signatures of within‐watershed gene flow; yet we also inferred at least two instances of cross‐watershed gene flow—one in the upstream reaches and one further downstream. The upstream cross‐watershed event appears to be very recent (41 ± 13 years), suggesting dispersal via recent flooding or undocumented human‐mediated transport. The downstream cross‐watershed event appears to be considerably older (577 ± 265 years), suggesting a role for rare geological or climatological events. Alongside these strong signatures of both contemporary and historical gene flow, we found little evidence of impacts on presumably adaptive phenotypic differentiation, except perhaps in the one instance of very recent cross‐watershed gene flow. Selection in this system seems to overpower gene flow—at least on the spatiotemporal scales investigated here.

Highlights

Historical and contemporary patterns of dispersal and gene flow are key components shaping population genetic structure (Bohonak, 1999; Slatkin, 1987)
Our goal will be to disen‐ tangle the roles of ongoing contemporary and historical gene flow in a classic evolutionary model system—Trinidadian guppies Poecilia reticulata (Peters, 1859)
To enable direct comparisons of population structure between the genetic and phenotypic data, we analyzed both types of data using discriminant analysis of principal components (DAPC; Jombart, Devillard, & Balloux, 2010) imple‐ mented in the R package adegenet

Summary

| INTRODUCTION

Historical and contemporary patterns of dispersal and gene flow are key components shaping population genetic structure (Bohonak, 1999; Slatkin, 1987). Exceptions are known wherein guppies occupying some tributaries in one watershed can show surprising genetic similarity to particular populations in other watersheds (Willing et al, 2010) These cross‐watershed affinities could reflect historical or contem‐ porary gene flow owing to natural events, such as earthquakes or severe flooding, or human‐mediated transport. Our goals were to (a) investigate population ge‐ netic structure of guppies in the two watersheds, (b) infer the ex‐ istence and timing of gene flow events between sites within and between watersheds, and (c) test for associations between gene flow and differences in male color. If inferred gene flow between watersheds was due to historical— and presumably rare—events, such as earthquakes or floods, esti‐ mated divergence times between sites should be older than a few centuries Deviations from this expectation (e.g., more recent di‐ vergence) would suggest the importance of contemporary fac‐ tors, such as recent natural or human‐mediated gene flow. Deviations from this ex‐ pectation (e.g., limited or no correspondence between neutral and adaptive divergence) would inform the extent to which local selection overcomes historical and contemporary gene flow, or would indicate genetic drift

| METHODS

| DISCUSSION

Findings

| CONCLUSION

CONFLICT OF INTEREST