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

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.

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

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.

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

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.

Genome-wide DNA methylation signatures of infection status in Trinidadian guppies (Poecilia reticulata).

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.

Offspring Hg exposure relates to parental feeding strategies in a generalist bird with strong individual foraging specialization.

Generalist species can potentially exploit a wide variety of resources, but at the individual level they often show a certain degree of foraging specialization. Specific foraging strategies, however, may increase exposure to environmental contaminants that can alter the cost-benefit balance of consuming particular food items. The Lesser Black-backed Gull (Larus fuscus) is known to opportunistically feed on a wide range of marine and terrestrial prey that differ in contaminant load, such as mercury (Hg) that strongly biomagnifies through the aquatic food web. The hypothesis tested in this study were: i) a predominant use of marine prey by females during egg-formation and by both parents during chick rearing increases the exposure to Hg during embryonic development and chick growth, and ii) this affects parental investment in clutch volume, chick growth and body condition. Total Hg burden and isotopic signatures of carbon (δ13C) and nitrogen (δ15N) were determined for eggs, down feathers, and primary feathers of L. fuscus chicks collected at a coastal colony in Belgium. As expected, eggs and feathers of chicks from parents with a stable isotope signature that suggested a predominantly marine diet had higher levels of Hg. The use of marine resources by females during the egg-formation period positively correlated to maternal investment in egg size, though entailing the cost of increased Hg-concentrations which in turn negatively affected clutch volume. Furthermore, it is shown that the use of chick down feathers is a suitable matrix to non-lethally estimate Hg concentrations in eggs. Contrary to our expectations, no relationship between Hg exposure and chick growth or chick body condition was found, which may be due the low concentrations found. We conclude that currently Hg contamination does not constitute a risk for development and condition of L. fuscus offspring at the levels currently observed at the Belgian coast.