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

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.

Asymmetric Isolation and the Evolution of Behaviors Influencing Dispersal: Rheotaxis of Guppies above Waterfalls

“…By contrast, the majority of studies on rheotaxis have focused on salmonids, which are typically migratory below (but not above) waterfalls, potentially favoring greater divergence in rheotaxis across such barriers than would be the case for non-migratory guppies. Second, the scale of our study might have been too small to detect any difference in rheotactic behavior: the sampled pools were only separated by 75 m for Aripo and 85 m for Turure, which is a scale on which downstream gene flow can be very high [33,55,56], potentially homogenizing adaptive variation. Furthermore, even though guppies sampled in the Turure were the most upstream site, this was not the case for the Aripo, which could also receive migrants from upstream.…”

Resistance and resilience of genetic and phenotypic diversity to “black swan” flood events: A retrospective analysis with historical samples of guppies

“…At the same time, gene flow in the downstream direction is limited by biotic factors, especially the general tendency of guppies to show positive rheotaxis, where they orient and swim upstream in a current (Blondel et al, 2020; Blondel et al, 2020; Mohammed et al, 2012). Yet this biotic resistance to the effects of water flow are sensitive to rare perturbations, such as stream capture events and human‐mediated introductions (Becher & Magurran, 2000; Blondel et al, 2019). Another such perturbation could be extreme floods, which are rare but potentially catastrophic.…”

Life histories as mosaics: plastic and genetic components differ among traits that underpin life-history strategies

“…Such differences should show up as variation among drainages in the amount of within-stream migration and in estimated divergence times between up-and downstream populations. Genetic analyses have confirmed these a posteriori hypotheses (Blondel et al 2019;Fraser et al 2015;Willing et al 2010).…”