Evolutionary adaptations by fish to ecotonal complexity in spatially variable landscapes — a perspective (original) (raw)
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Freshwater Biology
1. Recent findings highlighted the central role of the structure of the river network in shaping spatial patterns of genetic diversity in riverscapes. However, the influence of multiple anthropogenic stressors on these patterns may be just as important and the relative impacts of these two types of predictors have rarely been quantified simultaneously in river networks. Here, we contributed to filling this gap by investigating the relative contribution of both network structure and multiple anthropogenic stressors in shaping spatial patterns of genetic diversity in two freshwater fishes (Gobio occitaniae and Phoxinus phoxinus). 2. We focused on two rivers in which the two fish species were sampled along the upstream-downstream gradient. Microsatellite markers were used to quantify genetic diversity from three indices: allelic richness, private allelic richness and genetic uniqueness. Each sampling site was physically characterised according to its position in the network, and was described for multiple anthropogenic stressors including habitat degradation, fragmentation and stocking. This multiple-stressors approach was conducted using a fully explicit and generalisable analytical framework designed to cope with strong collinearity among environmental variables. 3. Overall, the contribution of network structure to the variance in genetic diversity was 1.8 times higher than the contribution of anthropogenic stressors. Both the position of sites along the upstream-downstream gradient and stocking were strong and consistent drivers of genetic variability. Conversely, the local influences of habitat degradation and fragmentation were species-and river-specific, sometimes even varying along the river channel, thus preventing any generalisations. 4. We concluded that the natural structure of networks and stocking strongly influence spatial patterns of genetic diversity in a predictable way, whereas the influence of other human activities may be much more difficult to predict over species and contexts.
Ecological genetics of freshwater fish: a short review of the genotype–phenotype connection
Animal Biodiversity and Conservation
Molecular ecology or ecological genetics is an expanding application of population genetics which has flourished in the last two decades but it is dominated by systematic and phylogeographic studies, with relatively little emphasis on the study of the genetic basis of the process of adaptation to different ecological conditions. The relationship between genotype and adaptive phenotypes is weak because populations are often difficult to quantify and experiments are logistically challenging or unfeasible. Interestingly, in freshwater fish, studies to characterize the genetic architecture of adaptive traits are not as rare as in other vertebrate groups. In this review, we summarize the few cases where the relationship between the ecology and genetics of freshwater fish is more developed, namely the relationship between genetic markers and ecological phenotypes.
2009
Landscape genetics holds promise for the forecasting of spatial patterns of genetic diversity based on key environmental features. Yet, the degree to which inferences based on single species can be extended to whole communities is not fully understood. We used a pristine and spatially structured community of three landlocked salmonids (Salvelinus fontinalis, Salmo salar, and Salvelinus alpinus) from Gros Morne National Park (Newfoundland, Canada) to test several predictions on the interacting effects of landscape and life history variation on genetic diversity, neutral divergence, and gene flow (m, migration rate). Landscape factors consistently influenced multispecies genetic patterns: (i) waterfalls created strong dichotomies in genetic diversity and divergence between populations above and below them in all three salmonids; (ii) contemporary m decreased with waterway distance in all three species, while neutral genetic divergence (h) increased with waterway distance, albeit in only two taxa; (iii) river flow generally produced downstream-biased m between populations when waterfalls separated these, but not otherwise. In contrast, we expected differential life history to result in a hierarchy of neutral divergence (S. salar > S. fontinalis > S. alpinus) based on disparities in dispersal abilities and population size from previous mark-recapture studies. Such hierarchy additionally matched varying degrees of spatial genetic structure among species revealed through individual-based analyses. We conclude that, whereas key landscape attributes hold power to predict multispecies genetic patterns in equivalent communities, they are likely to interact with species-specific life history attributes such as dispersal, demography, and ecology, which will in turn affect holistic conservation strategies.
Molecular Ecology, 2009
Conservation of species should be based on knowledge of effective population sizes and understanding of how breeding tactics and selection of recruitment habitats lead to genetic structuring. In the stream-spawning and genetically diverse brown trout, spawning and rearing areas may be restricted source habitats. Spatio-temporal genetic variability patterns were studied in brown trout occupying three lakes characterized by restricted stream habitat but high recruitment levels. This suggested non-typical lake-spawning, potentially representing additional spatio-temporal genetic variation in continuous habitats. Three years of sampling documented presence of young-of-the-year cohorts in littoral lake areas with groundwater inflow, confirming lake-spawning trout in all three lakes. Nine microsatellite markers assayed across 901 young-of-the-year individuals indicated overall substantial genetic differentiation in space and time. Nested gene diversity analyses revealed highly significant (≤ P = 0.002) differentiation on all hierarchical levels, represented by regional lakes (F LT = 0.281), stream vs. lake habitat within regional lakes (F HL = 0.045), sample site within habitats (F SH = 0.010), and cohorts within sample sites (F CS = 0.016). Genetic structuring was, however, different among lakes. It was more pronounced in a natural lake, which exhibited temporally stable structuring both between two lake-spawning populations and between lake-and stream spawners. Hence, it is demonstrated that lake-spawning brown trout form genetically distinct populations and may significantly contribute to genetic diversity. In another lake, differentiation was substantial between stream-and lake-spawning populations but not within habitat. In the third lake, there was less apparent spatial or temporal genetic structuring. Calculation of effective population sizes suggested small spawning populations in general, both within streams and lakes, and indicates that the presence of lake-spawning populations tended to reduce genetic drift in the total (meta-) population of the lake.
Global determinants of freshwater and marine fish genetic diversity
Nature Communications
Genetic diversity is estimated to be declining faster than species diversity under escalating threats, but its spatial distribution remains poorly documented at the global scale. Theory predicts that similar processes should foster congruent spatial patterns of genetic and species diversity, but empirical studies are scarce. Using a mined database of 50,588 georeferenced mitochondrial DNA barcode sequences (COI) for 3,815 marine and 1,611 freshwater fish species respectively, we examined the correlation between genetic diversity and species diversity and their global distributions in relation to climate and geography. Genetic diversity showed a clear spatial organisation, but a weak association with species diversity for both marine and freshwater species. We found a predominantly positive relationship between genetic diversity and sea surface temperature for marine species. Genetic diversity of freshwater species varied primarily across the regional basins and was negatively correl...
Assessing trait-environment relationships is crucial for predicting effects of natural andhuman-inducedenvironmentalchangeonbiota.Wecompiledaglobaldatabaseof fishassemblagesinestuaries,functionaltraitsoffishesandecosystemfeaturesofestuaries.Andwequantifiedtherelativeimportanceofecosystemfeaturesasdriversof patternsoffishfunctionaltraitsamongestuariesworldwide(i.e.driversoftheproportions of fish traits). In addition to biogeographical context, two main environmental gradientsregulatetraitspatterns:firstlytemperature,andsecondlyestuarysizeand hydrologicalconnectivityoftheestuarywiththemarineecosystem.Overall,estuaries incolderregions,withlargerareasandwithhigherhydrologicalconnectivitywiththe marineecosystem,havehigherproportionsofmarinefish(versusfreshwater),macrocarnivoresandplanktivores(versusomnivores,herbivoresanddetritivores)andlarger fish, with greater maximum depth of distribution andlongerlifespan. The observed trait patterns and trait-environment relationships are likely generated by multiple causalprocesseslinkedtophysiologicalconstraintsduetotemperatureandsalinity, size-dependent biotic interactions, as well as habitat availability and connectivity. Biogeographical context and environmental conditions drive species richness and composition,andpresentresultsshowthattheyalsodriveassemblagetraits.Theobserved trait patterns and trait-environment relationships suggest that assemblage composition is determined by the functional role of species within ecosystems. Conservationstrategiesshouldbecoordinatedgloballyandensureprotectionofan arrayofestuariesthatdifferinecosystemfeatures,evenifsomeofthoseestuariesdo notsupporthighspeciesrichness.
Landscape Ecology, 2006
Spatial and temporal landscape patterns have long been recognized to influence biological processes, but these processes often operate at scales that are difficult to study by conventional means. Inferences from genetic markers can overcome some of these limitations. We used a landscape genetics approach to test hypotheses concerning landscape processes influencing the demography of Lahontan cutthroat trout in a complex stream network in the Great Basin desert of the western US. Predictions were tested with population-and individual-based analyses of microsatellite DNA variation, reflecting patterns of dispersal, population stability, and local effective population sizes. Complementary genetic inferences suggested samples from migratory corridors housed a mixture of fish from tributaries, as predicted based on assumed migratory life histories in those habitats. Also as predicted, populations presumed to have greater proportions of migratory fish or from physically connected, large, or high quality habitats had higher genetic variability and reduced genetic differentiation from other populations. Populations thought to contain largely non-migratory individuals generally showed the opposite pattern, suggesting behavioral isolation. Estimated effective sizes were small, and we identified significant and severe genetic bottlenecks in several populations that were isolated, recently founded, or that inhabit streams that desiccate frequently. Overall, this work suggested that Lahontan cutthroat trout populations in stream networks are affected by a combination of landscape and metapopulation processes. Results also demonstrated that genetic patterns can reveal unexpected processes, even within a system that is well studied from a conventional ecological perspective.
Freshwater Biology, 2013
1. The biogeography of freshwater fish is determined in part by large-scale filters such as phylogenetic history, the spatial arrangement of catchments and environmental variability. Species are filtered from the regional pool if they possess a combination of functional traits enabling them to persist in the local environment. This article aims to quantify the relative importance of these large-scale filters in determining spatial variation in freshwater fish life-history traits and functional trait composition of Australian river basins. 2. We developed a database of 10 life-history traits for 141 native freshwater fish species and compiled species distribution data for 123 river basins across the Australian continent. In order to partition the variation in the representation of life-history trait into unique and overlapping components, we also quantified the degree of phylogenetic relatedness among species, the geographical arrangement of river basins throughout the landscape and 12 broad-scale environmental factors. We then related life-history trait composition to gradients of environmental variation by constrained multivariate ordination and simple linear regression. 3. Our explanatory matrices accounted for 86.8% of the total variation in life-history trait composition at the river basin scale, of which 59.4% could be attributed to phylogeny and spatially structured environmental variation. This component represents the overlap among the broad-scale filtering processes of phylogenetic history, spatial autocorrelation and environmental variability in accounting for the distribution of life-history traits across Australian river basins. 4. Our analysis showed strong associations between suites of life-history traits that define generation time and reproductive output and a strong climate-hydrological gradient across the landscape. We also showed significant correlations between specific environmental variables and a number of key life-history traits that highlight the importance of trait-mediated environmental filters at broad spatial scales. 5. This study advances our conceptual understanding of broad-scale community assembly theory and has revealed trait-environment relationships at scales relevant to restoration and conservation of aquatic biodiversity. Our study provides greater insight into the determinants of spatial variation in fish species distributions and potentially addresses key scientific challenges, such as understanding how fish communities are assembled, and identifies the potential threats to, and responses of, these communities caused by environmental change.
Ecological linkages between community and genetic diversity in zooplankton among boreal shield lakes
Ecology, 2009
Ecological linkages between species diversity in communities and genetic diversity in populations have potential to influence the assembly of communities in habitats recovering from human disturbance, but few studies have attempted to synthesize relationships between these levels of biological organization, especially for locally adapted species. No such studies have been done in freshwater ecosystems despite the plethora of environmental stressors plaguing aquatic communities around the world. We present the first study to test (1) whether diversity and dissimilarity among communities and populations of a locally adapted species are correlated and (2) whether communities and population haplotypes respond differently to environmental selection and spatial structure of habitats. We used a fragment of mitochondrial DNA (mtDNA) belonging to the gene cytochrome oxidase subunit I (COI) as a neutral tag to discriminate among different population haplotype variants. In boreal lakes with different histories of exposure to anthropogenic acidification, diversity and dissimilarity metrics for crustacean zooplankton communities and locally adapted populations of an abundant and broadly distributed calanoid copepod species, Leptodiaptomus minutus, did not correlate. This discord was likely because zooplankton communities responded more strongly to acidity and acidity-related environmental variables than spatial structure of lakes, whereas the distribution of L. minutus haplotypes was more strongly governed by spatial structure of lakes than environmental selection. Although spatial structure was the dominant driver of haplotype structure among L. minutus lake populations, there were similarities in the types of environmental variables that influenced the distributions of species in communities and haplotypes in populations. How haplotype diversity among populations relates to community diversity depends on the relative influence of spatial structure of habitats and selection at each of these scales of biological organization.