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The Genetic Architecture Underlying the Evolution of a Rare Piscivorous Life History Form in Brown Trout after Secondary Contact and Strong Introgression.

ABSTRACT: Identifying the genetic basis underlying phenotypic divergence and reproductive isolation is a longstanding problem in evolutionary biology. Genetic signals of adaptation and reproductive isolation are often confounded by a wide range of factors, such as variation in demographic history or genomic features. Brown trout (Salmo trutta) in the Loch Maree catchment, Scotland, exhibit reproductively isolated divergent life history morphs, including a rare piscivorous (ferox) life history form displaying larger body size, greater longevity and delayed maturation compared to sympatric benthivorous brown trout. Using a dataset of 16,066 SNPs, we analyzed the evolutionary history and genetic architecture underlying this divergence. We found that ferox trout and benthivorous brown trout most likely evolved after recent secondary contact of two distinct glacial lineages, and identified 33 genomic outlier windows across the genome, of which several have most likely formed through selection. We further identified twelve candidate genes and biological pathways related to growth, development and immune response potentially underpinning the observed phenotypic differences. The identification of clear genomic signals divergent between life history phenotypes and potentially linked to reproductive isolation, through size assortative mating, as well as the identification of the underlying demographic history, highlights the power of genomic studies of young species pairs for understanding the factors shaping genetic differentiation.

SUBMITTER: Jacobs A

PROVIDER: S-EPMC6026935 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The extraordinary polymorphism of major histocompatibility complex (MHC) genes is considered a paradigm of pathogen-mediated balancing selection, although empirical evidence is still scarce. Furthermore, the relative contribution of balancing selection to shape MHC population structure and diversity, compared to that of neutral forces, as well as its interaction with other evolutionary processes such as hybridization, remains largely unclear. To investigate these issues, we analyzed adaptive (MHC-DAB gene) and neutral (11 microsatellite loci) variation in 156 brown trout (Salmo trutta complex) from six wild populations in central Italy exposed to introgression from domestic hatchery lineages (assessed with the LDH gene). MHC diversity and structuring correlated with those at microsatellites, indicating the substantial role of neutral forces. However, individuals carrying locally rare MHC alleles/supertypes were in better body condition (a proxy of individual fitness/parasite load) regardless of the zygosity status and degree of sequence dissimilarity of MHC, hence supporting balancing selection under rare allele advantage, but not heterozygote advantage or divergent allele advantage. The association between specific MHC supertypes and body condition confirmed in part this finding. Across populations, MHC allelic richness increased with increasing admixture between native and domestic lineages, indicating introgression as a source of MHC variation. Furthermore, introgression across populations appeared more pronounced for MHC than microsatellites, possibly because initially rare MHC variants are expected to introgress more readily under rare allele advantage. Providing evidence for the complex interplay among neutral evolutionary forces, balancing selection, and human-mediated introgression in shaping the pattern of MHC (functional) variation, our findings contribute to a deeper understanding of the evolution of MHC genes in wild populations exposed to anthropogenic disturbance.

Project description:BACKGROUND:Estimates of fishing and natural mortality are important for understanding, and ultimately managing, commercial and recreational fisheries. High reward tags with fixed station acoustic telemetry provides a promising approach to monitoring mortality rates in large lake recreational fisheries. Kootenay Lake is a large lake which supports an important recreational fishery for large Bull Trout and Rainbow Trout. METHODS:Between 2008 and 2013, 88 large (?500 mm) Bull Trout and 149 large (?500 mm) Rainbow Trout were marked with an acoustic transmitter and/or high reward ($100) anchor tags in Kootenay Lake. The subsequent detections and angler recaptures were analysed using a Bayesian individual state-space Cormack-Jolly-Seber (CJS) survival model with indicator variable selection. RESULTS:The final CJS survival model estimated that the annual interval probability of being recaptured by an angler was 0.17 (95% CRI [0.11-0.23]) for Bull Trout and 0.14 (95% CRI [0.09-0.19]) for Rainbow Trout. The annual interval survival probability for Bull Trout was estimated to have declined from 0.91 (95% CRI [0.76-0.97]) in 2009 to just 0.46 (95% CRI [0.24-0.76]) in 2013. Rainbow Trout survival was most strongly affected by spawning. The annual interval survival probability was 0.77 (95% CRI [0.68-0.85]) for a non-spawning Rainbow Trout compared to 0.41 (95% CRI [0.30-0.53]) for a spawner. The probability of spawning increased with the fork length for both species and decreased over the course of the study for Rainbow Trout. DISCUSSION:Fishing mortality was relatively low and constant while natural mortality was relatively high and variable. The results indicate that angler effort is not the primary driver of short-term population fluctations in the Rainbow Trout abundance. Variation in the probability of Rainbow Trout spawning suggests that the spring escapement at the outflow of Trout Lake may be a less reliable index of abundance than previously assumed. Multi-species stock assessment models need to account for the fact that large Bull Trout are more abundant than large Rainbow Trout in Kootenay Lake.

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The Genetic Architecture Underlying the Evolution of a Rare Piscivorous Life History Form in Brown Trout after Secondary Contact and Strong Introgression.

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