A speciation gene for left–right reversal in snails results in anti-predator adaptation

How speciation genes can spread in a population is poorly understood. In land snails, a single gene for left–right reversal could be responsible for instant speciation, because dextral and sinistral snails have difficulty in mating. However, the traditional two-locus speciation model predicts that a mating disadvantage for the reversal should counteract this speciation. In this study, we show that specialized snake predation of the dextral majority drives prey speciation by reversal. Our experiments demonstrate that sinistral Satsuma snails (Stylommatophora: Camaenidae) survive predation by Pareas iwasakii (Colubroidea: Pareatidae). Worldwide biogeography reveals that stylommatophoran snail speciation by reversal has been accelerated in the range of pareatid snakes, especially in snails that gain stronger anti-snake defense and reproductive isolation from dextrals by sinistrality. Molecular phylogeny of Satsuma snails further provides intriguing evidence of repetitive speciation under snake predation. Our study demonstrates that a speciation gene can be fixed in populations by positive pleiotropic effects on survival

Geography-dependent horizontal gene transfer from vertebrate predators to their prey

Horizontal transfer (HT) of genes between multicellular animals, once thought to be extremely rare, is being more commonly detected, but its global geographic trend and transfer mechanism have not been investigated. We discovered a unique HT pattern of Bovine-B (BovB) LINE retrotransposons in vertebrates, with a bizarre transfer direction from predators (snakes) to their prey (frogs). At least 54 instances of BovB HT were detected, which we estimate to have occurred across time between 85 and 1.3 Ma. Using comprehensive transcontinental sampling, our study demonstrates that BovB HT is highly prevalent in one geographical region, Madagascar, suggesting important regional differences in the occurrence of HTs. We discovered parasite vectors that may plausibly transmit BovB and found that the proportion of BovB-positive parasites is also high in Madagascar where BovB thus might be physically transported by parasites to diverse vertebrates, potentially including humans. Remarkably, in two frog lineages, BovB HT occurred after migration from a non-HT area (Africa) to the HT hotspot (Madagascar). These results provide a novel perspective on how the prevalence of parasites influences the occurrence of HT in a region, similar to pathogens and their vectors in some endemic diseases

Evolution of a unique predatory feeding apparatus: functional anatomy, development and a genetic locus for jaw laterality in Lake Tanganyika scale-eating cichlids

Background While bilaterality is a defining characteristic of triploblastic animals, several assemblages have managed to break this symmetry in order to exploit the adaptive peaks garnered through the lateralization of behaviour or morphology. One striking example of an evolved asymmetry in vertebrates comes from a group of scale-eating cichlid fishes from Lake Tanganyika. Members of the Perissodini tribe of cichlid fishes have evolved dental and craniofacial asymmetries in order to more effectively remove scales from the left or right flanks of prey. Here we examine the evolution and development of craniofacial morphology and laterality among Lake Tanganyika scale-eating cichlids. Results Using both geometric and traditional morphometric methods we found that the craniofacial evolution in the Perissodini involved discrete shifts in skeletal anatomy that reflect differences in habitat preference and predation strategies. Further, we show that the evolutionary history of the Perissodini is characterized by an accentuation of craniofacial laterality such that certain taxa show elaborate sided differences in craniofacial shape consistent with the sub-partitioning of function between sides of the head during attacks. Craniofacial laterality in the scale-eating specialist Perissodus microlepis was found to be evident early in development and exhibited a unimodal distribution, which is contrary to the adult condition where jaw laterality has been described as a discrete, bimodal antisymmetry. Finally, using linkage and association analyses we identified a conserved locus for jaw handedness that segregates among East African cichlids. Conclusions We suggest that, during the evolution of the Perissodini, selection has accentuated a latent, genetically determined handedness of the craniofacial skeleton, enabling the evolution of jaw asymmetries in order to increase predation success. Continued work on the developmental genetic basis of laterality in the Perissodini will facilitate a better understanding of the evolution of this unique group of fishes, as well as of left-right axis determination among vertebrates in general

Molecular and cellular mechanisms underlying the evolution of form and function in the amniote jaw.

The amniote jaw complex is a remarkable amalgamation of derivatives from distinct embryonic cell lineages. During development, the cells in these lineages experience concerted movements, migrations, and signaling interactions that take them from their initial origins to their final destinations and imbue their derivatives with aspects of form including their axial orientation, anatomical identity, size, and shape. Perturbations along the way can produce defects and disease, but also generate the variation necessary for jaw evolution and adaptation. We focus on molecular and cellular mechanisms that regulate form in the amniote jaw complex, and that enable structural and functional integration. Special emphasis is placed on the role of cranial neural crest mesenchyme (NCM) during the species-specific patterning of bone, cartilage, tendon, muscle, and other jaw tissues. We also address the effects of biomechanical forces during jaw development and discuss ways in which certain molecular and cellular responses add adaptive and evolutionary plasticity to jaw morphology. Overall, we highlight how variation in molecular and cellular programs can promote the phenomenal diversity and functional morphology achieved during amniote jaw evolution or lead to the range of jaw defects and disease that affect the human condition

Evolution of whole-body enantiomorphy in the tree snail genus Amphidromus

Diverse animals exhibit left–right asymmetry in development. However, no example of dimorphism for the left–right polarity of development (whole-body enantiomorphy) is known to persist within natural populations. In snails, whole-body enantiomorphs have repeatedly evolved as separate species. Within populations, however, snails are not expected to exhibit enantiomorphy, because of selection against the less common morph resulting from mating disadvantage. Here we present a unique example of evolutionarily stable whole-body enantiomorphy in snails. Our molecular phylogeny of South-east Asian tree snails in the genus Amphidromus indicates that enantiomorphy has likely persisted as the ancestral state over a million generations. Enantiomorphs have continuously coexisted in every population surveyed spanning a period of 10 years. Our results indicate that whole-body enantiomorphy is maintained within populations opposing the rule of directional asymmetry in animals. This study implicates the need for explicit approaches to disclosure of a maintenance mechanism and conservation of the genus

Non-adaptive speciation of snails by left-right reversal is facilitated on oceanic islands

The nearly neutral theory of molecular evolution predicts that small population size is essential for non-adaptive evolution. Evolution of whole-body left-right reversal in snails is generally a compelling example of non-adaptive speciation, because variants with reversed chirality would suffer from reduced mating opportunities within a population. Despite this reproductive disadvantage, sinistral snail species have repeatedly originated from dextral ancestors in terrestrial pulmonates. Here I show that snail speciation by reversal has been accelerated on oceanic islands. Analysing the global biogeography of 995 genera across 84 stylommatophoran families, I found that the proportion of sinistral snail genera was enhanced in genera endemic to oceanic islands. Oceanic islands are relatively small land masses offering highly fragmented habitats for snails. Thus, the upper limit of population size would probably have been small for a long time there. Oceanic islands may have facilitated the fixation of the nonadaptive allele for speciation by reversal, allowing subsequent ecological divergence of sibling species. This study illustrates the potential role of genetic drift in non-adaptive speciation on oceanic islands