High gene flow despite opposite chirality in hybrid zones between enantiomorphic door snails

Abstract

We studied differentiation and geneflow patterns between enantiomorphic door-snail species in two hybrid zones in the Bucegi Mountains (Romania) to investigate the effects of intrinsic barriers (complications in copulation) and extrinsic selection by environmental factors. A mitochondrial gene tree confirmed the historical separation of the examined populations into the dextral Alopia livida and the sinistral Alopia straminicollis in accordance with the morphological classification, but also indicated gene flow between the species. By contrast, a network based on amplified fragment length polymorphisms (AFLP) markers revealed local groups of populations as units independent of their species affiliation. Admixture analyses based on AFLP data showed that the genomes of most individuals in the hybrid zones are composed of parts of the genomes of both parental taxa. The introgression patterns of a notable fraction of the examined markers deviated from neutral introgression. However, the patterns of most non-neutral markers were not concordant between the two hybrid zones. There was also no concordance between non-neutral markers in the two genomic clines and markers that were correlated with environmental variables or markers that were correlated with the proportion of dextral individuals in the populations. Neither extrinsic selection by environmental factors nor intrinsic barriers resulting from positive frequency-dependent selection of the prevailing coiling direction were sufficient to maintain the distinctness of A. straminicollis and A. livida. Despite being historically separated units, we conclude that these taxa now merge where they come into contact.

Patterns and processes in a non‐adaptive radiation: Alopia (Gastropoda, Clausiliidae) in the Bucegi Mountains

“…However, Nordsieck (, ) supposed that the two taxa hybridize only to a limited extent. In contrast, the admixture analyses of the nuclear markers (Figure ; see Koch et al, for additional analyses) showed that most specimens in the hybrid zones have a combination of similarly large components from the genomes of the parental taxa irrespective of their classification (Figure ; Koch et al, ). The introgression between the two taxa in the hybrid zones resulted in a fusion of their populations.…”

“…However, the gene flow estimates between A. livida nubila and A. straminicollis monacha and between A. livida hypula and A. s. straminicollis are higher than those between the taxa within the A. livida complex (Figure ). There is also frequent introgression of mitochondrial haplotypes (Figure ; Koch et al, ). The hybrid zones between A. livida and A. straminicollis in the Tatar Gorge and the Velican Valley were known based on morphological evidence (Nordsieck, ; Szekeres, , 2008, 2016).…”

“…Reversals of the primary asymmetry in spiral snails may affect gene flow because the position of the genital orifice on different body sides in dextral and sinistral snails can impede mating of differently coiled individuals (Asami, Cowie, & Ohbayashi, ; Johnson, ; Ueshima & Asami, ). It has been assumed that mutations of the gene determining the coiling direction might result even in single‐gene speciation (Gittenberger, ; Gittenberger, Hamann, & Asami, ; Orr, ; Ueshima & Asami, ; but see Johnson, Clarke, & Murray, ; Davison, Chiba, Barton, & Clarke, ; Koch, Neiber, Walther, & Hausdorf, ). Thus, reversals of the coiling direction may have contributed to the Alopia radiation.…”

“…Thus, reversals of the coiling direction may have contributed to the Alopia radiation. However, there is morphological (Nordsieck, ; Szekeres, ) as well as genetic (Koch et al, ) evidence for hybridization and introgression between differently coiled Alopia taxa in the Bucegi Mountains.…”

Evolution of a dextral lineage by left-right reversal inCristataria(Gastropoda, Pulmonata, Clausiliidae)

“…Clausiliids are high‐spired snails, which typically copulate by shell mounting. This type of copulation may not so severely restrict mating between the wild type and left–right reversed variant as face to face copulation in flat/globular stylommatophorans (Asami, Cowie, & Ohbayashi, ; Gittenberger, ; Koch, Neiber, Walther, & Hausdorf, ; Ueshima & Asami, ; Utsuno, Kasem, Fukuda, & Asami, ). Evolution of left–right reversed taxa has been more frequent in high‐spired pulmonate groups than in low‐spired groups, probably because of relaxation of positive frequency‐dependent selection against reversal in the former resulting from their possible interchiral copulation success (Asami et al., ; Gittenberger, ).…”