Genotype by sequencing identifies natural selection as a driver of intraspecific divergence in Atlantic populations of the high dispersal marine invertebrate, Macoma petalum

Abstract

Mitochondrial DNA analyses indicate that the Bay of Fundy population of the intertidal tellinid bivalve Macoma petalum is genetically divergent from coastal populations in the Gulf of Maine and Nova Scotia. To further examine the evolutionary forces driving this genetic break, we performed double digest genotype by sequencing (GBS) to survey the nuclear genome for evidence of both neutral and selective processes shaping this pattern. The resulting reads were mapped to a partial transcriptome of its sister species, M. balthica, to identify single nucleotide polymorphisms (SNPs) in protein‐coding genes. Population assignment tests, principle components analyses, analysis of molecular variance, and outlier tests all support differentiation between the Bay of Fundy genotype and the genotypes of the Gulf of Maine, Gulf of St. Lawrence, and Nova Scotia. Although both neutral and non‐neutral patterns of genetic subdivision were significant, genetic structure among the regions was nearly 20 times higher for loci putatively under selection, suggesting a strong role for natural selection as a driver of genetic diversity in this species. Genetic differences were the greatest between the Bay of Fundy and all other population samples, and some outlier proteins were involved in immunity‐related processes. Our results suggest that in combination with limited gene flow across the mouth of the Bay of Fundy, local adaptation is an important driver of intraspecific genetic variation in this marine species with high dispersal potential.

Genomic and Transcriptomic Differentiation of Independent Invasions of the Pacific Oyster Crassostrea gigas

“…The importance of galactose binding by C-type lectins was also reflected in the transcriptomes, where a galactose binding domain was annotated in eight differentially expressed genes. Together with the periodic enrichment of immune processes this confirms previous results (Wendling and Wegner, 2015;Bernardi et al, 2016;Metivier et al, 2017) and might suggest a higher importance of adaption in immune traits in invasions than previously expected (Cornet et al, 2016).…”

“…Also within species, some outlier loci differentiating invasive and native populations were associated with TEs in marine clams (Metivier et al, 2017). Extending these findings we could now detect TE-associated outlier loci between populations from independent invasions of another marine bivalve, which might suggest that transposon activation might be a more universal feature of successful invasion, and might be fine-tuned to the conditions encountered in newly colonized habitats.…”

“…Extending these findings we could now detect TE-associated outlier loci between populations from independent invasions of another marine bivalve, which might suggest that transposon activation might be a more universal feature of successful invasion, and might be fine-tuned to the conditions encountered in newly colonized habitats. Similar to outlier loci in clams (Metivier et al, 2017), the TE-associated loci identified here were silent or non-coding mutations suggesting that the outlier SNPs were not the direct target of natural selection. It is more likely that other genes changing their structure or expression as a consequence of transposon insertion might have conferred the selective advantage, and thus increased the frequency of TE-associated SNPs in a sweep like fashion.…”

“…It has been established as a pathogen associated molecular pattern (PAMP) recognized by C-type lectins in shellfish (Huang et al, 2013;Li et al, 2015), potentially suggesting a role in immune recognition of these genes. Immune genes are frequently found among outlier loci in invasive species (Bernardi et al, 2016;Metivier et al, 2017), highlighting the strength of diversifying selection exerted by the new set of pathogens invaders are exposed to after colonizing a new habitat (Wendling and Wegner, 2015). In fact, we could already show that the two oyster populations used here have evolved resistance against their sympatric communities of Vibrio spp.…”

Complex signatures of genomic variation of two non-model marine species in a homogeneous environment

“…Retroelements are highly mobile genetic elements that are known to play significant roles in disease progression, stress reactions and embryogenesis, and are thought to be found in regions of the genome with reduced rates of recombination [ 106 , 107 ]. Genes within these domains have been matched to outlier loci in previous genomic studies of other marine invertebrates [ 97 , 108 ], however, the authors of these studies conclude that this finding is not a result of the annotated sequences not being under selection themselves, but rather linked to loci that are under putative selection.…”