A new species of the genus Paradistomum (Platyhelminthes: Trematoda) from Iwasaki's snail-eating snake Pareas iwasakii, with a note on morphological variations of Paradistomum megareceptaculum (Tamura, 1941).

Dicrocoeliid trematodes were detected from Iwasaki's snail-eating snake Pareas iwasakii in Iriomote Island, Okinawa Prefecture, Japan, and described as a new species Paradistomum dextra n. sp. in the present study. This new species can be distinguished from the type series of the other members of the genus based on size of eggs and morphological characteristics of body, oral and ventral suckers, and reproductive organs. However, the new species was hard to distinguish from Paradistomum megareceptaculum infecting snakes in Japan, including Iriomote Island where is the type locality of the new species, because it is closely similar to some part of the broad range of morphological variations in P. megareceptaculum. On the other hand, a partial sequence of 28S ribosomal DNA clearly distinguished these two species. Moreover, the new species' host snake Pareas iwasakii is reported to exclusively feed on land snails while host snakes of P. megareceptaculum feed on small vertebrates, indicating that the new species is also ecologically different from P. megareceptaculum. We also redescribed P. megareceptaculum based on adults sampled in this study and past studies to record the morphological variations of this species.

Addressing the taxonomic confusion of Mesocoelium Odhner, 1910 (Trematoda: Plagiorchioidea: Mesocoeliidae) in Japanese urodelan and anuran amphibians.

Trematodes of the genus Mesocoelium Odhner, 1910 (Digenea: Plagiorchioidea: Mesocoeliidae) are globally distributed and parasitize amphibians, reptiles, or occasionally fishes. This genus is one of the most confusing taxa in trematodes because of its poor morphological features. In this study, we examined species of Mesocoelium collected from Japanese amphibians and found that they can be morphologically assigned to two species of Mesocoelium. Mesocoelium brevicaecum Ochi in Goto and Ozaki, 1929 parasitizes various both urodelan and anuran amphibians and occurred widely in Japan, while M. japonicum Goto and Ozaki, 1930 parasitizes a few hynobiid species in a limited part of Japan. We proposed ceca length as a valid key characteristic for species identification in this genus. M. elongatum Goto and Ozaki, 1929, M. lanceatum Goto and Ozaki, 1929, M. minutum Park, 1939, M. ovatum Goto and Ozaki, 1930, and M. pearsei Goto and Ozaki, 1930 are junior synonyms of M. brevicaecum, while M. japonicum can be distinguishable from them by morphologically and molecularly. Our molecular study supported the validity of both species and showed intraspecific divergence associated with geographic distance. Molecular identification suggests that the land snail Euhadra quaesita can serve as the first intermediate host for M. japonicum in Japan. This study also indicates the extremely low specificity of this genus for vertebrate hosts. Finally, we conclude that at least three species of Mesocoelium (M. brevicaecum, M. japonicum, and Mesocoelium sp. 1) are distributed in Japan. Further studies in other regions are undoubtedly required for a better understanding of the taxonomy and ecology of the genus Mesocoelium.

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.

Life-History Modeling Reveals the Ecological and Evolutionary Significance of Autotomy.

AbstractAutotomy, the self-amputation of body parts, serves as an antipredator defense in many taxonomic groups of animals. However, its adaptive value has seldom been quantified. Here, we propose a novel modeling approach for measuring the fitness advantage conferred by the capability for autotomy in the wild. Using a predator-prey system where a land snail autotomizes and regenerates its foot specifically in response to snake bites, we conducted a laboratory behavioral experiment and a 3-year multievent capture-mark-recapture study. Combining these empirical data, we developed a hierarchical model and estimated the basic life-history parameters of the snail. Using samples from the posterior distribution, we constructed the snail's life table as well as that of a snail variant incapable of foot autotomy. As a result of our analyses, we estimated the monthly encounter rate with snake predators at 3.3% (95% credible interval: 1.6%-4.9%), the contribution of snake predation to total mortality until maturity at 43.3% (15.0%-95.3%), and the fitness advantage conferred by foot autotomy at 6.5% (2.7%-11.5%). This study demonstrated the utility of the multimethod hierarchical-modeling approach for the quantitative understanding of the ecological and evolutionary processes of antipredator defenses in the wild.

Asymmetry of mandibular dentition is associated with dietary specialization in snail-eating snakes.

BACKGROUND: In vertebrates, the left-and-right pairs of homologous organs are generally present in equal numbers. A remarkable exception is snail-eating snakes in the family Pareidae: almost all the pareid snakes have much more teeth on the right mandible than on the left for functional specialization in feeding on the dextral majority of land snails. Because the only exceptional species with symmetric dentition has been regarded as a slug-eater, the extent of dietary specialization on slugs could shape the degree of the lateral asymmetry of mandibular dentition (dentition asymmetry) even among snail eaters. METHODS: To test this, I compared the morphology and behavior of two sympatric species of Taiwanese snail-eating snakes, Pareas atayal and P. formosensis. RESULTS: Specimens collected in the same locality showed that the dentition asymmetry of P. formosensis was significantly smaller than that of P. atayal. Congruent to its weak asymmetry, P. formosensis showed a strong preference of slugs to snails in the feeding experiment. DISCUSSION: The dietary specialization of P. formosensis on slugs would contribute to niche partitioning from the sympatric congener P. atayal. This study suggests that the diverse variation in the dentition asymmetry of pareid snakes is the result of their dietary specialization and divergence.

Roles of maternal effects in maintaining genetic variation: Maternal storage effect.

Understanding the maintenance of genetic variation remains a central challenge in evolutionary biology. Recent empirical studies suggest the importance of temporally varying selection, as allele frequencies have been found to fluctuate substantially in the wild. However, previous theory suggests that the conditions for the maintenance of genetic variation under temporally fluctuating selection are quite restrictive. Using mathematical models, we demonstrate that maternal genetic effects, whereby maternal genotypes affect offspring phenotypes, can facilitate the maintenance of polymorphism in temporally varying environments. Maternal effects result in mismatches between genotypes and phenotypes, thereby buffering the influence of selection on allele frequency. This decreases the magnitude of allele-frequency fluctuations and creates conditions for the maintenance of variation when selection causes fluctuations. Therefore, maternal effects may result in a temporal storage effect ("maternal storage effect"). On the other hand, when selection does not cause fluctuations (e.g., linear negative frequency-dependent selection), maternal genetic effects moderate the relative importance of selection compared to genetic drift and promote stochastic allele extinction in finite populations. Thus, maternal effects can play an important role in the maintenance of polymorphism, but the direction of the effect depends on the nature of selection.

Mitochondrial genomes of Japanese Babina frogs (Ranidae, Anura): unique gene arrangements and the phylogenetic position of genus Babina.

Genus Babina is a member of Ranidae, a large family of frogs, currently comprising 10 species. Three of them are listed as endangered species. To identify mitochondrial (mt) genes suitable for future population genetic analyses for endangered species, we determined the complete nucleotide sequences of the mt genomes of 3 endangered Japanese Babina frogs, B. holsti, B. okinavana, and B. subaspera and 1 ranid frog Lithobates catesbeianus. The genes of NADH dehydrogenase subunit 5 (nad5) and the control region (CR) were found to have high sequence divergences and to be usable for population genetics studies. At present, no consensus on the phylogenetic position of genus Babina has been reached. To resolve this problem, we performed molecular phylogenetic analyses with the largest dataset used to date (11,345 bp from 2 ribosomal RNA- and 13 protein-encoding genes) in studies dealing with Babina phylogeny. These analyses revealed monophyly of Babina and Odorrana. It is well known that mt gene rearrangements of animals can provide usable phylogenetic information. Thus, we also compared the mt gene arrangements among Babina species and other related genera. Of the surveyed species, only L. catesbeianus manifested typical neobatrachian-type mt gene organization. In the B. okinavana, an additional pseudogene of tRNA-His (trnH) was observed in the CR downstream region. Furthermore, in the B. holsti and B. subaspera, the trnH/nad5 block was translocated from its typical position to the CR downstream region, and the translocated trnH became a pseudogene. The position of the trnH pseudogene is consistent with the translocated trnH position reported in Odorrana. Consequently, the trnH rearrangement seems to be a common ancestry characteristic (synapomorphy) of Babina and Odorrana. Based on the "duplication and deletion" gene rearrangement model, a single genomic duplication event can explain the order of derived mt genes found in Babina and Odorrana.

Cost of autotomy drives ontogenetic switching of anti-predator mechanisms under developmental constraints in a land snail.

Autotomy of body parts offers various prey animals immediate benefits of survival in compensation for considerable costs. I found that a land snail Satsuma caliginosa of populations coexisting with a snail-eating snake Pareas iwasakii survived the snake predation by autotomizing its foot, whereas those out of the snake range rarely survived. Regeneration of a lost foot completed in a few weeks but imposed a delay of shell growth. Imprints of autotomy were found in greater than 10 per cent of S. caliginosa in the snake range but in only less than 1 per cent out of it, simultaneously demonstrating intense predation by the snakes and high efficiency of autotomy for surviving snake predation in the wild. However, in experiments, mature S. caliginosa performed autotomy less frequently. Instead of the costly autotomy, they can use defensive denticles on the inside of their shell apertures. Owing to the constraints from the additive growth of shells, most pulmonate snails can produce these denticles only when they have fully grown up. Thus, this developmental constraint limits the availability of the modified aperture, resulting in ontogenetic switching of the alternative defences. This study illustrates how costs of adaptation operate in the evolution of life-history strategies under developmental constraints.

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.

Divergent shell shape as an antipredator adaptation in tropical land snails.

Although many land snails exhibit amazingly divergent shell shapes in the tropics, the functions of these remain obscure. Here we show that a modified aperture shape acts as an impediment specifically to predation by a snail-eating snake. Pareas iwasakii (Colubridae: Pareatinae) uses a unique method to feed on land snails: the snake extracts the soft body from the shell through the aperture by alternately retracting its mandibles. The snail Satsuma caliginosa (Camaenidae: Camaeninae) has apertural variation in regard to the presence of snail-eating snakes. Our experiments demonstrated that the distorted aperture mechanically impeded predation by this gape-limited predator, interrupting the mandibular movements. In contrast, congeneric snails with round apertures did not escape predation by snakes. The paleobiogeography of the focal area indicates that the subspecies Satsuma caliginosa picta, which does not have apertural modification, was derived from a defensive ancestor after the extinction of snail-eating snakes. Our study suggests a possibility that snail-eating snakes are responsible for divergent shell shapes in a variety of tropical land snails.

Right-handed snakes: convergent evolution of asymmetry for functional specialization.

External asymmetry found in diverse animals bears critical functions to fulfil ecological requirements. Some snail-eating arthropods exhibit directional asymmetry in their feeding apparatus for foraging efficiency because dextral (clockwise) species are overwhelmingly predominant in snails. Here, we show convergence of directional asymmetry in the dentition of snail-eating vertebrates. We found that snakes in the subfamily Pareatinae, except for non-snail-eating specialists, have more teeth on the right mandible than the left. In feeding experiments, a snail-eating specialist Pareas iwasakii completed extracting a dextral soft body faster with fewer mandible retractions than a sinistral body. The snakes failed in holding and dropped sinistral snails more often owing to behavioural asymmetry when striking. Our results demonstrate that symmetry break in dentition is a key innovation that has opened a unique ecological niche for snake predators.