Whole-genome sequencing illuminates multifaceted targets of selection to humic substances in Eurasian perch

Extreme environments are inhospitable to the majority of species, but some organisms are able to survive in such hostile conditions due to evolutionary adaptations. For example, modern bony fishes have colonized various aquatic environments, including perpetually dark, hypoxic, hypersaline and toxic habitats. Eurasian perch (Perca fluviatilis) is among the few fish species of northern latitudes that is able to live in very acidic humic lakes. Such lakes represent almost "nocturnal" environments; they contain high levels of dissolved organic matter, which in addition to creating a challenging visual environment, also affects a large number of other habitat parameters and biotic interactions. To reveal the genomic targets of humic-associated selection, we performed whole-genome sequencing of perch originating from 16 humic and 16 clear-water lakes in northern Europe. We identified over 800,000 single nucleotide polymorphisms, of which >10,000 were identified as potential candidates under selection (associated with >3000 genes) using multiple outlier approaches. Our findings suggest that adaptation to the humic environment may involve hundreds of regions scattered across the genome. Putative signals of adaptation were detected in genes and gene families with diverse functions, including organism development and ion transportation. The observed excess of variants under selection in regulatory regions highlights the importance of adaptive evolution via regulatory elements, rather than via protein sequence modification. Our study demonstrates the power of whole-genome analysis to illuminate the multifaceted nature of humic adaptation and provides the foundation for further investigation of causal mutations underlying phenotypic traits of ecological and evolutionary importance

Zooplanktivore fish body growth responses to browning-induced light limitation vary over ontogeny, but not with fish density

Ongoing climate change is leading to browning of many lakes and coastal areas, which can impair fish body growth and biomass production. However, whether and how effects of light limitation caused by browning on fish body growth vary over early ontogeny is unknown. In this study, we set up a mesocosm experiment to test whether roach (Rutilus rutilus) body growth responses to browning depend on body size, and if findings are robust over roach densities. We also studied a potential mechanism for size-specific responses by conducting an aquaria experiment to test if size-specific prey selectivity in roach changes with browning. We found that roach body growth responses to browning-induced light limitation vary over ontogeny (independent of roach density), negatively affecting body growth of young-of-the-year (YOY) but not of 1-year-old individuals. We also show that this difference in growth response is likely a consequence of browning-induced alterations in zooplankton community composition and variation in prey selectivity between YOY and 1-year-old fish. This suggests that we should account for the diverse effects of browning over fish ontogeny, mediated via altered prey composition and ontogenetic changes in prey preference, when assessing overall impacts of browning on aquatic ecosystems

Data from: Intraspecific phenotypic variation among alewife populations drives parallel phenotypic shifts in bluegill

Evolutionary diversification within consumer species may generate selection on local ecological communities, affecting prey community structure. However, the extent to which this niche construction can propagate across food webs and shape trait variation in competing species is unknown. Here, we tested whether niche construction by different life-history variants of the planktivorous fish alewife (Alosa pseudoharengus) can drive phenotypic divergence and resource use in the competing species bluegill (Lepomis macrochirus). Using a combination of common garden experiments and a comparative field study, we found that bluegill from landlocked alewife lakes grew relatively better when fed small than large zooplankton, had gill rakers better adapted for feeding on small-bodied prey and selected smaller zooplankton compared with bluegill from lakes with anadromous or no alewife. Observed shifts in bluegill foraging traits in lakes with landlocked alewife parallel those in alewife, suggesting interspecific competition leading to parallel phenotypic changes rather than to divergence (which is commonly predicted). Our findings suggest that species may be locally adapted to prey communities structured by different life-history variants of a competing dominant species

Data to Huss et al 2014

Experimental data on bluegill growth rates and prey size. Comparative lake data on bluegill gill raker morphology

Warmer and browner waters decrease fish biomass production

Climate change studies have long focused on effects of increasing temperatures, often without considering other simultaneously occurring environmental changes, such as browning of waters. Resolving how the combination of warming and browning of aquatic ecosystems affects fish biomass production is essential for future ecosystem functioning, fisheries, and food security. In this study, we analyzed individual- and population-level fish data from 52 temperate and boreal lakes in Northern Europe, covering large gradients in water temperature and color (absorbance, 420 nm). We show that fish (Eurasian perch, Perca fluviatilis) biomass production decreased with both high water temperatures and brown water color, being lowest in warm and brown lakes. However, while both high temperature and brown water decreased fish biomass production, the mechanisms behind the decrease differed: temperature affected the fish biomass production mainly through a decrease in population standing stock biomass, and through shifts in size- and age-distributions toward a higher proportion of young and small individuals in warm lakes; brown water color, on the other hand, mainly influenced fish biomass production through negative effects on individual body growth and length-at-age. In addition to these findings, we observed that the effects of temperature and brown water color on individual-level processes varied over ontogeny. Body growth only responded positively to higher temperatures among young perch, and brown water color had a stronger negative effect on body growth of old than on young individuals. Thus, to better understand and predict future fish biomass production, it is necessary to integrate both individual- and population-level responses and to acknowledge within-species variation. Our results suggest that global climate change, leading to browner and warmer waters, may negatively affect fish biomass production, and this effect may be stronger than caused by increased temperature or water color alone

Warmer and browner waters decrease fish biomass production

Climate change studies have long focused on effects of increasing temperatures,often without considering other simultaneously occurring environmental changes, such as browning of waters. Resolving how the combination of warming and browning of aquatic ecosystems affects fish biomass production is essential for future ecosystem functioning, fisheries, and food security. In this study, we analyzed individual‐ and population‐level fish data from 52 temperate and boreal lakes in Northern Europe, covering large gradients in water temperature and color (absorbance, 420 nm). We show that fish (Eurasian perch, Perca fluviatilis) biomass production decreased with both high water temperatures and brown water color, being lowest in warm and brown lakes. However, while both high temperature and brown water decreased fish biomass production, the mechanisms behind the decrease differed: temperature affected the fish biomass production mainly through a decrease in population standing stock biomass, and through shifts in size‐ and age‐distributions toward a higher proportion of young and small individuals in warm lakes; brown water color, on the other hand, mainly influenced fish biomass production through negative effects on individual body growth and length‐at‐ age. In addition to thesefindings, we observed that the effects of temperature and brown water color onindividual‐level processes varied over ontogeny. Body growth only responded positively to higher temperatures among young perch, and brown water color had a stronger negative effect on body growth of old than on young individuals. Thus, to better understand and predict future fish biomass production, it is necessary to integrate both individual‐ and population‐level responses and to acknowledge within species variation. Our results suggest that global climate change, leading to browner and warmer waters, may negatively affect fish biomass production, and this effect may be stronger than caused by increased temperature or water color alone<br/

Appendix A. Details on functions, parameters, and analyses.

Details on functions, parameters, and analyses

Predators with multiple ontogenetic niche shifts have limited potential for population growth and top-down control of their prey

Catastrophic collapses of top predators have revealed trophic cascades and community structuring by top-down control. When populations fail to recover after a collapse, this may indicate alternative stable states in the system. Overfishing has caused several of the most compelling cases of these dynamics, and in particular Atlantic cod stocks exemplify such lack of recovery. Often, competition between prey species and juvenile predators is hypothesized to explain the lack of recovery of predator populations. The predator is then considered to compete with its prey for one resource when small and to subsequently shift to piscivory. Yet predator life history is often more complex than that, including multiple ontogenetic diet shifts. Here we show that no alternative stable states occur when predators in an intermediate life stage feed on an additional resource (exclusive to the predator) before switching to piscivory, because predation and competition between prey and predator do not simultaneously structure community dynamics. We find top-down control by the predator only when there is no feedback from predator foraging on the additional resource. Otherwise, the predator population dynamics are governed by a bottleneck in individual growth occurring in the intermediate life stage. Therefore, additional resources for predators may be beneficial or detrimental for predator population growth and strongly influence the potential for top-down community control.This study is part of the PLAN FISH project, financially supported by the Swedish Environmental Protection Agency and the Swedish Board of Fisheries.</p