Diving into broad-scale and high-resolution population genomics to decipher drivers of structure and climatic vulnerability in a marine invertebrate.

Species with widespread distributions play a crucial role in our understanding of climate change impacts on population structure. In marine species, population structure is often governed by both high connectivity potential and selection across strong environmental gradients. Despite the complexity of factors influencing marine populations, studying species with broad distribution can provide valuable insights into the relative importance of these factors and the consequences of climate-induced alterations across environmental gradients. We used the northern shrimp Pandalus borealis and its wide latitudinal distribution to identify current drivers of population structure and predict the species' vulnerability to climate change. A total of 1514 individuals sampled across 24° latitude were genotyped at high geographic (54 stations) and genetic (14,331 SNPs) resolutions to assess genetic variation and environmental correlations. Four populations were identified in addition to finer substructure associated with local adaptation. Geographic patterns of neutral population structure reflected predominant oceanographic currents, while a significant proportion of the genetic variation was associated with gradients in salinity and temperature. Adaptive landscapes generated using climate projections suggest a larger genomic offset in the southern extent of the P. borealis range, where shrimp had the largest adaptive standing genetic variation. Our genomic results combined with recent observations point to further deterioration in southern regions and an impending vulnerable status in the regions at higher latitudes for P. borealis. They also provide rare insights into the drivers of population structure and climatic vulnerability of a widespread meroplanktonic species, which is crucial to understanding future challenges associated with invertebrates essential to ecosystem functioning.

Harvest is associated with the disruption of social and fine-scale genetic structure among matrilines of a solitary large carnivore.

Harvest can disrupt wildlife populations by removing adults with naturally high survival. This can reshape sociospatial structure, genetic composition, fitness, and potentially affect evolution. Genetic tools can detect changes in local, fine-scale genetic structure (FGS) and assess the interplay between harvest-caused social and FGS in populations. We used data on 1614 brown bears, Ursus arctos, genotyped with 16 microsatellites, to investigate whether harvest intensity (mean low: 0.13 from 1990 to 2005, mean high: 0.28 from 2006 to 2011) caused changes in FGS among matrilines (8 matrilines; 109 females ≥4 years of age), sex-specific survival and putative dispersal distances, female spatial genetic autocorrelation, matriline persistence, and male mating patterns. Increased harvest decreased FGS of matrilines. Female dispersal distances decreased, and male reproductive success was redistributed more evenly. Adult males had lower survival during high harvest, suggesting that higher male turnover caused this redistribution and helped explain decreased structure among matrilines, despite shorter female dispersal distances. Adult female survival and survival probability of both mother and daughter were lower during high harvest, indicating that matriline persistence was also lower. Our findings indicate a crucial role of regulated harvest in shaping populations, decreasing differences among "groups," even for solitary-living species, and potentially altering the evolutionary trajectory of wild populations.

Offspring mass variation in tree swallows: A case of bet-hedging?

The evolution of reproductive strategies is affected by the ability of organisms to deal with future environmental conditions. When environments are temporally unpredictable, however, it is difficult to anticipate optimal offspring phenotype. Diversification of offspring phenotypes, a strategy called diversified bet-hedging, may allow parents to maximize their fitness by reducing between-year variation in reproductive success. The link between diversification of offspring phenotypes and individual reproductive success, however, has rarely been documented empirically. We used an eight-year dataset (1215 broods, 870 females) on individually marked tree swallows (Tachycineta bicolor) to assess whether intra-brood mass variation was compatible with a diversified bet-hedging strategy. Intra-brood mass variation was weakly, but significantly repeatable within females, suggesting consistent individual differences. Greater intra-brood mass variation, however, was not associated with reduced between-year variation in reproductive success or increased female reproductive success. Moreover, contrary to diversified bet-hedging expectations, fledging success of large broods was greater when hatchlings had similar rather than variable masses. Our results suggest that intra-brood mass variation may not result from diversified bet-hedging, but rather from complex interactions between environmental, brood, and maternal characteristics.

Effects of blood parasite infection and innate immune genetic diversity on mating patterns in a passerine bird breeding in contrasted habitats.

Genetic diversity at immune genes and levels of parasitism are known to affect patterns of (dis)assortative mating in several species. Heterozygote advantage and/or good genes should shape mate choice originating from pathogen/parasite-driven selection at immune genes. However, the stability of these associations, and whether they vary with environmental conditions, are still rarely documented. In this study, we describe mating patterns in a wild population of tree swallows (Tachycineta bicolor) over 4 years and assess the effects of haemosporidian parasite infection and immune genetic diversity at ß-defensin genes on those patterns within two habitats of contrasting environmental quality, in southern Québec, Canada. We first show that mating patterns were only very weakly related to individual status of infection by haemosporidian parasites. However, we found a difference between habitats in mating patterns related to infection status, which was likely due to a non-random distribution of individuals, as non-infected mating pairs were more frequent in lower quality habitats. Mating patterns also differed depending on ß-defensin heterozygosity at AvBD2, but only for genetic partners outside of the social couple, with heterozygous individuals pairing together. Our study underlines the importance of considering habitat heterogeneity in studies of sexual selection.

Multidimensional environmental influences on timing of breeding in a tree swallow population facing climate change.

Most phenological traits are extremely sensitive to current climate change, and advances in the timing of important life-history events have been observed in many species. In birds, phenotypic plasticity in response to temperature is thought to be the main mechanism underlying yearly adjustment in the timing of breeding. However, other factors could be important and interact to affect the levels of plastic responses between and/or within-individuals. Here, we use long-term individual-based data on tree swallow (Tachycineta bicolor) to identify the spatial and environmental drivers affecting plasticity in laying date and to assess their importance at both population and individual levels. We found that laying date has advanced by 4.2 days over 10 years, and that it was mainly influenced by latitude and an interaction between spring temperature and breeder density. Analyses of individual plasticity showed that increases in temperature, but not in breeder density, resulted in within-individual advances in laying date. Our results suggest that females can adjust their laying date as a function of temperature, but that this adjustment will be partly constrained in habitats with lower breeder densities. Such potential constraint is especially worrying for the broad array of species already declining as a result of climate change.

Candidate gene-environment interactions and their relationships with timing of breeding in a wild bird population.

Monitoring and predicting evolutionary changes underlying current environmental modifications are complex challenges. Recent approaches to achieve these objectives include assessing the genetic variation and effects of candidate genes on traits indicating adaptive potential. In birds, for example, short tandem repeat polymorphism at four candidate genes (CLOCK, NPAS2, ADCYAP1, and CREB1) has been linked to variation in phenological traits such as laying date and timing of migration. However, our understanding of their importance as evolutionary predictors is still limited, mainly because the extent of genotype-environment interactions (GxE) related to these genes has yet to be assessed. Here, we studied a population of Tree swallow (Tachycineta bicolor) over 4 years in southern Québec (Canada) to assess the relationships between those four candidate genes and two phenological traits related to reproduction (laying date and incubation duration) and also determine the importance of GxE in this system. Our results showed that NPAS2 female genotypes were nonrandomly distributed across the study system and formed a longitudinal cline with longer genotypes located to the east. We observed relationships between length polymorphism at all candidate genes and laying date and/or incubation duration, and most of these relationships were affected by environmental variables (breeding density, latitude, or temperature). In particular, the positive relationships detected between laying date and both CLOCK and NPAS2 female genotypes were variable depending on breeding density. Our results suggest that all four candidate genes potentially affect timing of breeding in birds and that GxE are more prevalent and important than previously reported in this context.

Intraspecific genetic admixture and the morphological diversification of an estuarine fish population complex.

The North-east American Rainbow smelt (Osmerus mordax) is composed of two glacial races first identified through the spatial distribution of two distinct mtDNA lineages. Contemporary breeding populations of smelt in the St. Lawrence estuary comprise contrasting mixtures of both lineages, suggesting that the two races came into secondary contact in this estuary. The overall objective of this study was to assess the role of intraspecific genetic admixture in the morphological diversification of the estuarine rainbow smelt population complex. The morphology of mixed-ancestry populations varied as a function of the relative contribution of the two races to estuarine populations, supporting the hypothesis of genetic admixture. Populations comprising both ancestral mtDNA races did not exhibit intermediate morphologies relative to pure populations but rather exhibited many traits that exceeded the parental trait values, consistent with the hypothesis of transgressive segregation. Evidence for genetic admixture at the level of the nuclear gene pool, however, provided only partial support for this hypothesis. Variation at nuclear AFLP markers revealed clear evidence of the two corresponding mtDNA glacial races. The admixture of the two races at the nuclear level is only pronounced in mixed-ancestry populations dominated by one of the mtDNA lineages, the same populations showing the greatest degree of morphological diversification and population structure. In contrast, mixed-ancestry populations dominated by the alternate mtDNA lineage showed little evidence of introgression of the nuclear genome, little morphological diversification and little contemporary population genetic structure. These results only partially support the hypothesis of transgressive segregation and may be the result of the differential effects of natural selection acting on admixed genomes from different sources.

Drawing ecological inferences from coincident patterns of population- and community-level biodiversity.

Biodiversity is comprised of genetic and phenotypic variation among individual organisms, which might belong to the same species or to different species. Spatial patterns of biodiversity are of central interest in ecology and evolution for several reasons: to identify general patterns in nature (e.g. species-area relationships, latitudinal gradients), to inform conservation priorities (e.g. identifying hotspots, prioritizing management efforts) and to draw inferences about processes, historical or otherwise (e.g. adaptation, the centre of origin of particular clades). There are long traditions in ecology and evolutionary biology of examining spatial patterns of biodiversity among species (i.e. in multispecies communities) and within species, respectively, and there has been a recent surge of interest in studying these two types of pattern simultaneously. The idea is that examining both levels of diversity can materially advance the above-stated goals and perhaps lead to entirely novel lines of inquiry. Here, we review two broad categories of approach to merging studies of inter- and intraspecific variation: (i) the study of phenotypic trait variation along environmental gradients and (ii) the study of relationships between patterns of molecular genetic variation within species and patterns of distribution and diversity across species. For the latter, we report a new meta-analysis in which we find that correlations between species diversity and genetic diversity are generally positive and significantly stronger in studies with discrete sampling units (e.g. islands, lakes, forest fragments) than in studies with nondiscrete sampling units (e.g. equal-area study plots). For each topic, we summarize the current state of knowledge and key future directions.