Ecological Speciation and the Intertidal Snail <i>Littorina saxatilis</i>

Galindo, Juan; Grahame, J.

doi:10.1155/2014/239251

Cited by 17 publications

(15 citation statements)

References 47 publications

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“…Lastly, fluctuation in levels of admixture observed in this study compared to the study conducted by Galindo et al. () may support variation in temporal and spatial exogenous barriers to gene flow Galindo et al, . Phenotypically intermediate individuals may still represent individuals of mixed genetic background, but hybridization between ecotypes may have occurred several generations ago, allowing time for selection against the crab ecotype genetic background.…”

Section: Discussionsupporting

confidence: 64%

Genomic divergence between Spanish Littorina saxatilis ecotypes unravels limited admixture and extensive parallelism associated with population history

Kess

Galindo

Boulding

2018

Ecology and Evolution

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The rough periwinkle, Littorina saxatilis, is a model system for studying parallel ecological speciation in microparapatry. Phenotypically parallel wave‐adapted and crab‐adapted ecotypes that hybridize within the middle shore are replicated along the northwestern coast of Spain and have likely arisen from two separate glacial refugia. We tested whether greater geographic separation corresponding to reduced opportunity for contemporary or historical gene flow between parallel ecotypes resulted in less parallel genomic divergence. We sequenced double‐digested restriction‐associated DNA (ddRAD) libraries from individual snails from upper, mid, and low intertidal levels of three separate sites colonized from two separate refugia. Outlier analysis of 4256 SNP markers identified 34.4% sharing of divergent loci between two geographically close sites; however, these sites each shared only 9.9%–15.1% of their divergent loci with a third more‐distant site. STRUCTURE analysis revealed that genotypes from only three of 166 phenotypically intermediate mid‐shore individuals appeared to result from recent hybridization, suggesting that hybrids cannot be reliably identified using shell traits. Hierarchical AMOVA indicated that the primary source of genomic differentiation was geographic separation, but also revealed greater similarity of the same ecotype across the two geographically close sites than previously estimated with dominant markers. These results from a model system for ecological speciation suggest that genomic parallelism is affected by the opportunity for historical or contemporary gene flow between populations.

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Section: Discussionsupporting

confidence: 64%

Genomic divergence between Spanish Littorina saxatilis ecotypes unravels limited admixture and extensive parallelism associated with population history

Kess

Galindo

Boulding

2018

Ecology and Evolution

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“…One of the best characterized models for unravelling these evolutionary processes in the intertidal zone is the gastropod Littorina saxatilis . In this species, several pairs of ecotypes seem to have independently evolved across multiple geographic regions from local populations under similar divergent selective pressures (crab predation and wave exposure), resulting in parallel evolution of reproductive isolation (Butlin et al ., ; Galindo & Grahame, ).…”

Section: Introductionmentioning

confidence: 99%

“…The phenotypic differences between these Iberian forms could have resulted from the distinct selective pressures they experience. For instance, the small shell size of the ME ecotype could represent an adaptation to avoid wave dislodgement, as suggested for the small exposed ecotype (SU) of L. saxatilis from Iberia (Johannesson, Johannesson & Rolán‐Alvarez, ; Rolán‐Alvarez, Johannesson & Erlandsson, ; and reviewed by Galindo & Grahame, ), whereas cryptic shell colour could have evolved as an antipredator strategy (Reimchen, ; Rolán & Templado, ). However, to our knowledge, the degree of local adaptation of these forms has not yet been properly evaluated (e.g.…”

Section: Introductionmentioning

confidence: 99%

Genetic characterization of flat periwinkles (Littorinidae) from the Iberian Peninsula reveals interspecific hybridization and different degrees of differentiation

Carvalho

Sotelo

Galindo

et al. 2016

Biol. J. Linn. Soc.

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The flat periwinkles, Littorina fabalis and L. obtusata, are two intertidal gastropods that offer a promising system for local adaptation and ecological speciation studies. Taking advantage of 17 recently developed specific microsatellite loci, we performed the first comprehensive genetic characterization of these sister species in the Iberian Peninsula. Special attention was given to L. fabalis by sampling populations representing the three morphotypes/ecotypes described from the region, which mainly differ in the habitat they are confined to (i.e. algae/seagrass 'host' species and level of wave exposure). Our analysis revealed, for the first time, the existence of hybrids between L. fabalis and L. obtusata in a natural population, which suggests that despite their strong genetic differentiation, reproductive isolation is not complete. Furthermore, the differentiation between L. fabalis ecotypes is lower than between these and L. obtusata; and their population genetic structure appears to be mainly governed by geography. However, ecological and demographic factors seem to have also played an important role, as suggested by the higher population differentiation in one of the ecotypes. Altogether, this work provides an important baseline for further studies on flat periwinkles as a model to explore how reproductive barriers evolve and interact with each other across a speciation continuum.

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“…We find evidence of: (a) polygenic architecture of differentiated shell shape and size traits, (b) elevated linkage of QTL associated with shell variation despite a genome‐wide distribution, and (c) partial overlap of divergent F ST outlier regions associated with shape variation detected during genome‐wide association, suggesting increased rates of divergence at QTL underlying shell variation. Together these results from an empirical study of an emerging model system (Ravinet et al, ; Galindo & Grahame, ) present a complex illustration of genomic architecture evolution during ecological speciation, revealing variable patterns of allelic differentiation and genome‐wide linkage during adaptation.…”

Section: Discussionmentioning

confidence: 78%

Genome‐wide association analyses reveal polygenic genomic architecture underlying divergent shell morphology in SpanishLittorina saxatilisecotypes

Kess

Boulding

2019

Ecology and Evolution

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Gene flow between diverging populations experiencing dissimilar ecological conditions can theoretically constrain adaptive evolution. To minimize the effect of gene flow, alleles underlying traits essential for local adaptation are predicted to be located in linked genome regions with reduced recombination. Local reduction in gene flow caused by selection is expected to produce elevated divergence in these regions. The highly divergent crab‐adapted and wave‐adapted ecotypes of the marine snail Littorina saxatilis present a model system to test these predictions. We used genome‐wide association (GWA) analysis of geometric morphometric shell traits associated with microgeographic divergence between the two L. saxatilis ecotypes within three separate sampling sites. A total of 477 snails that had individual geometric morphometric data and individual genotypes at 4,066 single nucleotide polymorphisms (SNPs) were analyzed using GWA methods that corrected for population structure among the three sites. This approach allowed dissection of the genomic architecture of shell shape divergence between ecotypes across a wide geographic range, spanning two glacial lineages. GWA revealed 216 quantitative trait loci (QTL) with shell size or shape differences between ecotypes, with most loci explaining a small proportion of phenotypic variation. We found that QTL were evenly distributed across 17 linkage groups, and exhibited elevated interchromosomal linkage, suggesting a genome‐wide response to divergent selection on shell shape between the two ecotypes. Shell shape trait‐associated loci showed partial overlap with previously identified outlier loci under divergent selection between the two ecotypes, supporting the hypothesis of diversifying selection on these genomic regions. These results suggest that divergence in shell shape between the crab‐adapted and wave‐adapted ecotypes is produced predominantly by a polygenic genomic architecture with positive linkage disequilibrium among loci of small effect.

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Ecological Speciation and the Intertidal Snail Littorina saxatilis

Cited by 17 publications

References 47 publications

Genomic divergence between Spanish Littorina saxatilis ecotypes unravels limited admixture and extensive parallelism associated with population history

Genomic divergence between Spanish Littorina saxatilis ecotypes unravels limited admixture and extensive parallelism associated with population history

Genetic characterization of flat periwinkles (Littorinidae) from the Iberian Peninsula reveals interspecific hybridization and different degrees of differentiation

Genome‐wide association analyses reveal polygenic genomic architecture underlying divergent shell morphology in SpanishLittorina saxatilisecotypes

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