Atlantic herring is an excellent species for studying the genetic basis of adaptation in geographically distant populations because of its characteristically large population sizes and low genetic drift. In this study we compared whole-genome resequencing data of Atlantic herring populations from both sides of the Atlantic Ocean. An important finding was the very low degree of genetic differentiation among geographically distant populations (fixation index = 0.026), suggesting lack of reproductive isolation across the ocean. This feature of the Atlantic herring facilitates the detection of genetic factors affecting adaptation because of the sharp contrast between loci showing genetic differentiation resulting from natural selection and the low background noise resulting from genetic drift. We show that genetic factors associated with timing of reproduction are shared between genetically distinct and geographically distant populations. The genes for thyroidstimulating hormone receptor (TSHR), the SOX11 transcription factor (SOX11), calmodulin (CALM), and estrogen receptor 2 (ESR2A), all with a significant role in reproductive biology, were among the loci that showed the most consistent association with spawning time throughout the species range. In fact, the same two SNPs located at the 5′ end of TSHR showed the most significant association with spawning time in both the east and west Atlantic. We also identified unexpected haplotype sharing between spring-spawning oceanic herring and autumn-spawning populations across the Atlantic Ocean and the Baltic Sea. The genomic regions showing this pattern are unlikely to control spawning time but may be involved in adaptation to ecological factor(s) shared among these populations.genetic adaptation | Atlantic herring | parallel evolution | reproductive strategies | whole-genome resequencing
Knowing how many individuals there are in a population is a fundamental problem in the management and conservation of freshwater and marine fish. We compare abundance estimates (census size, Nc) in seven brook trout Salvelinus fontinalis populations using standard mark–recapture (MR) and the close‐kin mark–recapture (CKMR) method. Our purpose is to validate CKMR as a method for estimating population size. Close‐kin mark–recapture is based on the principle that an individual's genotype can be considered a “recapture” of the genotypes of each of its parents. Assuming offspring and parents are sampled independently, the number of parent–offspring pairs (POPs) genetically identified in these samples can be used to estimate abundance. We genotyped (33 microsatellites) and aged c. 2,400 brook trout individuals collected over 5 consecutive years (2014–2018). We provide an alternative interpretation of CKMR in terms of the Lincoln–Petersen estimator in which the parents are considered as tagging the offspring rather than the offspring “recapturing” the parents. Despite various sources of uncertainty, we find close agreement between standard MR abundance estimates obtained through double‐pass electrofishing and CKMR estimates, which require information on age‐specific fecundity, and population‐ and age‐specific survival rates. Population sizes (trueN^) are estimated to range between 300 and 6,000 adult individuals. Our study constitutes the first in situ validation of CKMR and establishes it as a useful method for estimating population size in aquatic systems where assumptions of random sampling and thorough mixing of individuals can be met.
Anadromous, resident, and landlocked Arctic char (Salvelinus alpinus) differentially experience drift and gene flow, making them ideal for studying incipient divergence. We investigated genetic divergence within and among char occupying landlocked and sea-accessible sites in Labrador, Canada, using 11 microsatellites. Unlike anadromous char, landlocked char were highly genetically differentiated. Genetic subgroups were detected within landlocked and sea-accessible sites. Within Ramah Lake (a sea-accessible site containing two subgroups), one subgroup matured at a small size, and both subgroups had equal proportions of males to females. These findings refute residency as a sneaker male tactic and instead suggest the presence of reproductively isolated resident and anadromous char. Subgroups demonstrated equal frequencies of Atlantic and Arctic lineage mtDNA haplotypes, suggesting their genetic differences were not due to allopatry during the last glacial maximum. Our results are therefore consistent with the sympatric genetic divergence of resident and anadromous Arctic char morphs.
The relationship between the effective number of breeders ( N b ) and the generational effective size ( N e ) has rarely been examined empirically in species with overlapping generations and iteroparity. Based on a suite of 11 microsatellite markers, we examine the relationship between N b , N e and census population size ( N c ) in 14 brook trout ( Salvelinus fontinalis ) populations inhabiting 12 small streams in Nova Scotia and sampled at least twice between 2009 and 2015. Unbiased estimates of N b obtained with individuals of a single cohort, adjusted on the basis of age at first maturation ( α ) and adult lifespan (AL), were from 1.66 to 0.24 times the average estimates of N e obtained with random samples of individuals of mixed ages (i.e. ). In turn, these differences led to adjusted N e estimates that were from nearly five to 0.7 times the estimates derived from mixed-aged individuals. These differences translate into the same range of variation in the ratio of effective to census population size within populations. Adopting as the more precise and unbiased estimates, we found that these brook trout populations differ markedly in their effective to census population sizes (range approx. 0.3 to approx. 0.01). Using A ge N e , we then showed that the variance in reproductive success or reproductive skew varied among populations by a factor of 40, from V k / k ≈ 5 to 200. These results suggest wide differences in population dynamics, probably resulting from differences in productivity affecting the intensity of competition for access to mates or redds, and thus reproductive skew. Understanding the relationship between N e , N b and N c , and how these relate to population dynamics and fluctuations in population size, are important for the design of robust conservation strategies in small populations with overlapping generations and iteroparity.
The genetic underpinnings of incipient speciation, including the genomic mechanisms which contribute to morphological and ecological differentiation and reproductive isolation, remain poorly understood. The repeated evolution of consistently, phenotypically distinct morphs of Arctic Charr (Salvelinus alpinus) within the Quaternary period offer an ideal model to study the repeatability of evolution at the genomic level. Sympatric morphs of Arctic Charr are found across this species' circumpolar distribution. However, the specific genetic mechanisms driving this morph differentiation are largely unknown despite the cultural and economic importance of the anadromous morph. We used a newly designed 87k SNP chip to investigate the character and consistency of the genomic differences among sympatric morphs within three recently deglaciated and geographically proximate lakes in Labrador, Canada. We found genetically distinct small and large morph Arctic Charr in all three lakes consistent with resident and anadromous morphs, respectively. A degree of reproductive isolation among sympatric morphs is likely given genome‐wide distributions of outlier SNPs and high genome‐wide FSTs. Across all lakes, outlier SNPs were largely nonoverlapping suggesting a lack of genetic parallelism driving morph differentiation. Alternatively, several genes and paralogous copies of the same gene consistently differentiated morphs across multiple lakes suggesting their importance to the manifestation of morphs. Our results confirm the utility of Arctic Charr as a model for investigating the predictability of evolution and support the importance of both genetic parallelism and nonparallelism to the incipient speciation of Arctic Charr morphs.
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