Epigenetic modification, especially DNA methylation, can play an important role in mediating gene regulatory response to environmental stressors and may be a key process affecting phenotypic plasticity and adaptation. Parasites are potent stressors with profound physiological and ecological effects on their hosts, yet it remains unclear how parasites influence host methylation patterns. Here, we used a well-studied host-parasite system, the guppy Poecilia reticulata and its ectoparasitic monogenean Gyrodactylus turnbulli to gain mechanistic insight into the dynamics of DNA methylation in host-parasite interactions. To explore this, we quantitatively measured genome-wide DNA methylation in guppy skin tissue using reduced representation bisulphite sequencing and characterized differential methylation patterns in guppies during distinct phases of infection. We identified 365, 313, and 741 differentially methylated regions (DMRs) between infected and control fish in early infection, peak infection and recovery phases, respectively. The magnitude of the methylation difference was moderate in DMRs, with an average of 29% (early infection), 27% (peak infection) and 30% (recovery) differential methylation per DMR. Approximately 50% of DMRs overlapped with CpG islands, and over half of the DMRs overlapped with gene bodies, several of which encode proteins relevant to immune response. These findings provide the first evidence of an epigenetic signature of infection by ectoparasites and demonstrate the changing relationship between epigenetic variation and immune response in distinct phases of infection.
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.
Populations that are asymmetrically isolated, such as above waterfalls, can sometimes export emigrants in a direction from which they do not receive immigrants, and thus provide an excellent opportunity to study the evolution of dispersal traits. We investigated the rheotaxis of guppies above barrier waterfalls in the Aripo and Turure rivers in Trinidad-the later having been introduced in 1957 from a below-waterfall population in another drainage. We predicted that, as a result of strong selection against downstream emigration, both of these above-waterfall populations should show strong positive rheotaxis. Matching these expectations, both populations expressed high levels of positive rheotaxis, possibly reflecting contemporary (rapid) evolution in the introduced Turure population. However, the two populations used different behaviors to achieve the same performance of strong positive rheotaxis, as has been predicted in the case of multiple potential evolutionary solutions to the same functional challenge (i.e., "many-to-one mapping"). By contrast, we did not find any difference in rheotactic behavior above versus below waterfalls on a small scale within either river, suggesting constraints on adaptive divergence on such scales.
Rare extreme “black swan” disturbances can impact ecosystems in many ways, such as destroying habitats, depleting resources, and causing high mortality. In rivers, for instance, exceptional floods that occur infrequently (e.g., so‐called “50‐year floods”) can strongly impact the abundance of fishes and other aquatic organisms. Beyond such ecological effects, these floods could also impact intraspecific diversity by elevating genetic drift or dispersal and by imposing strong selection, which could then influence the population's ability to recover from disturbance. And yet, natural systems might be resistant (show little change) or resilient (show rapid recovery) even to rare extreme events – perhaps as a result of selection due to past events. We considered these possibilities in two rivers where native guppies experienced two extreme floods – one in 2005 and another in 2016. For each river, we selected four sites and used archived “historical” samples to compare levels of genetic and phenotypic diversity before vs. after floods. Genetic diversity was represented by 33 neutral microsatellite markers, and phenotypic diversity was represented by body length and male melanic (black) colour. We found that genetic diversity and population structure was mostly “resistant” to even these extreme floods; whereas the larger impacts on phenotypic diversity were short‐lived, suggesting additional “resilience”. We discuss the determinants of these two outcomes for guppies facing floods, and then consider the general implications for the resistance and resilience of intraspecific variation to black swan disturbances.
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