Milk provisioning in oviparous caecilian amphibians.

Among vertebrates, the yolk is commonly the only form of nutritional investment offered by the female to the embryo. Some species, however, have developed parental care behaviors associated with specialized food provisioning essential for offspring survival, such as the production of lipidic-rich parental milk in mammals. Here, we show that females of the egg-laying caecilian amphibian Siphonops annulatus provide similarly lipid-rich milk to altricial hatchlings during parental care. We observed that for 2 months, S. annulatus babies ingested milk released through the maternal vent seemingly in response to tactile and acoustic stimulation by the babies. The milk, composed mainly of lipids and carbohydrates, originates from the maternal oviduct epithelium's hypertrophied glands. Our data suggest lactation in this oviparous nonmammalian species and expand the knowledge of parental care and communication in caecilians.

Milk provisioning in oviparous caecilian amphibians

Among vertebrates, the yolk is commonly the only form of nutritional investment offered by the female to the embryo. Some species, however, have developed parental care behaviors associated with specialized food provisioning essential for offspring survival, such as the production of lipidic-rich parental milk in mammals. Here, we show that females of the egg-laying caecilian amphibian Siphonops annulatus provide similarly lipid-rich milk to altricial hatchlings during parental care. We observed that for 2 months, S. annulatus babies ingested milk released through the maternal vent seemingly in response to tactile and acoustic stimulation by the babies. The milk, composed mainly of lipids and carbohydrates, originates from the maternal oviduct epithelium’s hypertrophied glands. Our data suggest lactation in this oviparous nonmammalian species and expand the knowledge of parental care and communication in caecilians.

Explaining reviewing effort: Existing reviews as potential driver.

Online review systems try to motivate reviewers to invest effort in writing reviews, as their success crucially depends on the helpfulness of such reviews. Underlying cognitive mechanisms, however, might influence future reviewing effort. Accordingly, in this study, we analyze whether existing reviews matter for future textual reviews. From analyzing a dataset from Google Maps covering 40 sights across Europe with over 37,000 reviews, we find that textual reviewing effort, as measured by the propensity to write an optional textual review and (textual) review length, is negatively related to the number of existing reviews. However, and against our expectations, reviewers do not increase textual reviewing effort if there is a large discrepancy between the existing rating valence and their own rating. We validate our findings using additional review data from Yelp. This work provides important implications for online platforms with review systems, as the presentation of review metrics matters for future textual reviewing effort.

Morphology of the Cutaneous Poison and Mucous Glands in Amphibians with Particular Emphasis on Caecilians (Siphonops annulatus).

Caecilians (order Gymnophiona) are apodan, snake-like amphibians, usually with fossorial habits, constituting one of the most unknown groups of terrestrial vertebrates. As in orders Anura (frogs, tree frogs and toads) and Caudata (salamanders and newts), the caecilian skin is rich in mucous glands, responsible for body lubrication, and poison glands, producing varied toxins used in defence against predators and microorganisms. Whereas in anurans and caudatans skin gland morphology has been well studied, caecilian poison glands remain poorly elucidated. Here we characterised the skin gland morphology of the caecilian Siphonops annulatus, emphasising the poison glands in comparison to those of anurans and salamanders. We showed that S. annulatus glands are similar to those of salamanders, consisting of several syncytial compartments full of granules composed of protein material but showing some differentiated apical compartments containing mucus. An unusual structure resembling a mucous gland is frequently observed in lateral/apical position, apparently connected to the main duct. We conclude that the morphology of skin poison glands in caecilians is more similar to salamander glands when compared to anuran glands that show a much-simplified structure.

Morphology of the cutaneous poison and mucous glands in amphibians with particular emphasis on caecilians (Siphonops annulatus)

Caecilians (order Gymnophiona) are apodan, snake-like amphibians, usually with fossorial habits, constituting one of the most unknown groups of terrestrial vertebrates. As in orders Anura (frogs, tree frogs and toads) and Caudata (salamanders and newts), the caecilian skin is rich in mucous glands, responsible for body lubrication, and poison glands, producing varied toxins used in defence against predators and microorganisms. Whereas in anurans and caudatans skin gland morphology has been well studied, caecilian poison glands remain poorly elucidated. Here we characterised the skin gland morphology of the caecilian Siphonops annulatus, emphasising the poison glands in comparison to those of anurans and salamanders. We showed that S. annulatus glands are similar to those of salamanders, consisting of several syncytial compartments full of granules composed of protein material but showing some differentiated apical compartments containing mucus. An unusual structure resembling a mucous gland is frequently observed in lateral/apical position, apparently connected to the main duct. We conclude that the morphology of skin poison glands in caecilians is more similar to salamander glands when compared to anuran glands that show a much-simplified structure.

Osteology of the Italian endemic spectacled salamanders, Salamandrina spp. (Amphibia, Urodela, Salamandridae): selected skeletal elements for palaeontological investigations.

Salamandrina perspicillata, from Northern and Central Italy, and Salamandrina terdigitata, from Southern Italy, represent a unique case of endemism among the amphibians of Europe. Some efforts were made to study the biology and ecology of these species, but only few studies focused on their comparative osteology. In particular, detailed descriptions of isolated skeletal elements and comparisons with other European urodeles are not available in literature hindering the identification of their fossils that testify for an ancient much broader range. The correct identification of fossil remains, mostly based on careful osteological descriptions, is fundamental to study the evolution of the range of this genus through time and the origin of the current endemic condition. This work is focused on the description of selected skeletal elements (occipito-otic complex, limb bones, atlas, trunk, sacral, caudosacral and caudal vertebrae) of dry-prepared skeletons and CT-scans of wet preserved specimens, which are the most common in the fossil record. We provide osteological comparison of Salamandrina with other genera of Europe, yielding diagnostic characters which allow the identification of fossils at a generic level. No significant differences between the two species S. perspicillata and S. terdigitata were found in the described skeletal elements, thus, the identification of skeletal elements at the species level is, at the moment, impossible.

Cranial shape evolution of extant and fossil crocodile newts and its relation to reproduction and ecology.

The diversity of the vertebrate cranial shape of phylogenetically related taxa allows conclusions on ecology and life history. As pleurodeline newts (the genera Echinotriton, Pleurodeles and Tylototriton) have polymorphic reproductive modes, they are highly suitable for following cranial shape evolution in relation to reproduction and environment. We investigated interspecific differences externally and differences in the cranial shape of pleurodeline newts via two-dimensional geometric morphometrics. Our analyses also included the closely related but extinct genus Chelotriton to better follow the evolutionary history of cranial shape. Pleurodeles was morphologically distinct in relation to other phylogenetically basal salamanders. The subgenera within Tylototriton (Tylototriton and Yaotriton) were well separated in morphospace, whereas Echinotriton resembled the subgenus Yaotriton more than Tylototriton. Oviposition site choice correlated with phylogeny and morphology. Only the mating mode, with a random distribution along the phylogenetic tree, separated crocodile newts into two morphologically distinct groups. Extinct Chelotriton likely represented several species and were morphologically and ecologically more similar to Echinotriton and Yaotriton than to Tylototriton subgenera. Our data also provide the first comprehensive morphological support for the molecular phylogeny of pleurodeline newts.

On the taxonomic status of Lygosoma (Keneuxia) dubium Werner, 1909.

The species Lygosoma (Keneuxia) dubium was described by Franz Werner (1909) based on a single specimen from the Royal Natural History Cabinet (Königliches Naturalienkabinett) in Stuttgart, collection number 3651. According to the original description the specimen was collected by "Direktor Mayer" in Yokohama, Japan in 1897. Much later Nakamura Ueno (1963) transferred the species to the Genus Dasia Gray, 1839, without further comments. Recently Uetz et al. (2018) questioned the type locality given by Werner (1909) and suggested that the name Lygosoma dubium is likely to be a synonym of Dasia grisea (Gray, 1845) referring to a personal comment of T. Hikida in 2014. However the actual taxonomic status of the species still remains unresolved.

Life history and reproduction of the neotropical caecilian Siphonops annulatus (Amphibia, Gymnophiona, Siphonopidae), with special emphasis on parental care

Due to their mainly fossorial way of life, caecilian amphibians are the least known order of terrestrial vertebrates. Here, we present new observations on the natural history and reproductive biology of the neotropical oviparous, siphonopid caecilian Siphonops annulatus from a long-term study of this species in the field and in captivity. In the studied population, mating occurs between the end of August and beginning of October, and oviposition between November and December, when rainfall peaks. Egg hatching occurs between the end of December and beginning of January. The complete cycle of maternal care, from oviposition to independent, self-sufficient offspring lasts about 3 months. After eclosion, the altricial young feed on the mother's specially modified skin (maternal dermatophagy) and are also supplied by a fluid released from coming from the maternal cloaca. Also presented are observations on the burrows, feeding and social behaviour of S. annulatus.

Life history and reproduction of the neotropical caecilian Siphonops annulatus (Amphibia, Gymnophiona, Siphonopidae), with special emphasis on parental care

Due to their mainly fossorial way of life, caecilian amphibians are the least known order of terrestrial vertebrates. Here, we present new observations on the natural history and reproductive biology of the neotropical oviparous, siphonopid caecilian Siphonops annulatus from a long-term study of this species in the field and in captivity. In the studied population, mating occurs between the end of August and beginning of October, and oviposition between November and December, when rainfall peaks. Egg hatching occurs between the end of December and beginning of January. The complete cycle of maternal care, from oviposition to independent, self-sufficient offspring lasts about 3 months. After eclosion, the altricial young feed on the mother's specially modified skin (maternal dermatophagy) and are also supplied by a fluid released from coming from the maternal cloaca. Also presented are observations on the burrows, feeding and social behaviour of S. annulatus.

Flesh and bone: An integrative approach towards sexual size dimorphism of a terrestrial salamander (genus Salamandrina).

Males and females face different selection pressures due to a sexually biased investment into reproduction. This often results in different morphologies. Sexual size dimorphisms (SSD) can give us important hints on the evolution and biology of a species. Salamanders are a perfectly suited system for investigating SSD, including a diversity of reproductive modes and behaviors, and patterns of SSD combined with life history traits in a phylogenetic context help us to understand the evolution of these processes. Because spectacled salamanders (genus Salamandrina) are the phylogenetically most basal taxon of the Salamandridae, they play a key role in reconstructing the evolutionary pattern of SSD. Combining extensive external and skeletal measurements of the cranium, limbs, and the pelvic girdle using high-resolution micro Computer Tomography (µCT) yielded an integrative analysis of expressed SSD of morphology and osteology of Salamandrina perspicillata. Multivariate analysis of external characters showed that males generally had larger cloacae, heads, and limbs relative to body size, while females had larger trunks. Analysis of osteology confirmed this pattern but also revealed new dimorphic characters in the cranium and the pelvic girdle. Dimorphic characters in external morphology and osteology are likely linked to the different reproductive roles of the sexes and support sexual rather than ecological selection as the primary force acting on the phenotype of the phylogenetically basal salamandrids.

Phylotranscriptomic consolidation of the jawed vertebrate timetree.

Phylogenomics is extremely powerful but introduces new challenges as no agreement exists on "standards" for data selection, curation and tree inference. We use jawed vertebrates (Gnathostomata) as model to address these issues. Despite considerable efforts in resolving their evolutionary history and macroevolution, few studies have included a full phylogenetic diversity of gnathostomes and some relationships remain controversial. We tested a novel bioinformatic pipeline to assemble large and accurate phylogenomic datasets from RNA sequencing and find this phylotranscriptomic approach successful and highly cost-effective. Increased sequencing effort up to ca. 10Gbp allows recovering more genes, but shallower sequencing (1.5Gbp) is sufficient to obtain thousands of full-length orthologous transcripts. We reconstruct a robust and strongly supported timetree of jawed vertebrates using 7,189 nuclear genes from 100 taxa, including 23 new transcriptomes from previously unsampled key species. Gene jackknifing of genomic data corroborates the robustness of our tree and allows calculating genome-wide divergence times by overcoming gene sampling bias. Mitochondrial genomes prove insufficient to resolve the deepest relationships because of limited signal and among-lineage rate heterogeneity. Our analyses emphasize the importance of large curated nuclear datasets to increase the accuracy of phylogenomics and provide a reference framework for the evolutionary history of jawed vertebrates.

Sexual dimorphism and age of Mediterranean salamanders.

We analysed sexual size dimorphism (SSD) for two Mediterranean species of the "true" salamander clade possessing distinct life histories (Salamandra algira and Mertensiella caucasica) and equilibrated the morphometric approach to individual age by using skeletochronology. For species that have a short breeding season and live at high altitudes, such as Mediterranean amphibians, the fecundity advantage hypothesis predicts female-biased SSD to maximise reproductive success. Our results showed no SSD in either species; however, morphometric data indicated a male-biased dimorphism in limb (arm and leg) dimensions in both species when compared to body size. Limb dimorphisms are likely related to the particular mating system, which involves an amplexus during spermatophore transfer. Arm length appeared sexually dimorphic during ontogeny both in viviparous S. algira and oviparous M. caucasica. A review on SSD indicated monomorphy of body size as a common lineage-specific pattern among the "true" salamander clade, but also the common presence of other traits such as sexually dimorphic limb proportions.

Sperm storage in caecilian amphibians.

BACKGROUND: Female sperm storage has evolved independently multiple times among vertebrates to control reproduction in response to the environment. In internally fertilising amphibians, female salamanders store sperm in cloacal spermathecae, whereas among anurans sperm storage in oviducts is known only in tailed frogs. Facilitated through extensive field sampling following historical observations we tested for sperm storing structures in the female urogenital tract of fossorial, tropical caecilian amphibians. FINDINGS: In the oviparous Ichthyophis cf. kohtaoensis, aggregated sperm were present in a distinct region of the posterior oviduct but not in the cloaca in six out of seven vitellogenic females prior to oviposition. Spermatozoa were found most abundantly between the mucosal folds. In relation to the reproductive status decreased amounts of sperm were present in gravid females compared to pre-ovulatory females. Sperm were absent in females past oviposition. CONCLUSIONS: Our findings indicate short-term oviductal sperm storage in the oviparous Ichthyophis cf. kohtaoensis. We assume that in female caecilians exhibiting high levels of parental investment sperm storage has evolved in order to optimally coordinate reproductive events and to increase fitness.

Sexual size dimorphism in caecilian amphibians: analysis, review and directions for future research.

Sexual dimorphism, widespread in the animal kingdom, describes differences between the sexes in size, shape and many other traits. Sexual size dimorphism (SSD) plays a significant role in understanding life history evolution and mating systems. The snakelike morphology of limbless caecilian amphibians lacking obvious secondary sexual characters (in contrast to frogs and salamanders) impedes accurate intrasexual comparisons. In this study, sexual size dimorphism in the oviparous caecilian Ichthyophis cf. kohtaoensis, a phylogenetically basal caecilian, was analysed. Females were larger in all body and head characters tested. However, when adjusted to body size (total length), females differed only in their cloacal shape. Clutch volume was positively correlated to female body size, thus female fecundity increased with body size supporting the hypothesis of a fecundity-selected SSD in the oviparous Ichthyophis cf. kohtaoensis. A review of the present SSD data for caecilians shows that many species are monomorphic for body size but show dimorphism in head size, while other species demonstrate female-biased SSD. Male-biased SSD has not been reported for caecilians. To understand life history evolution in caecilians, further studies on the reproductive biology of other taxa are urgently needed, in particular for rhinatrematids and uraeotyphlids. New data will allow phylogenetically controlled comparative analyses to fully explore the pattern of SSD among caecilian lineages.

Care and parentage in a skin-feeding caecilian amphibian.

An exceptional form of parental care has recently been discovered in a poorly known caecilian amphibian. Mothers of the Taita Hills (Kenya) endemic Boulengerula taitanus provide their own skin as a food source for their offspring. Field data suggest that nursing is costly. Females found attending young had a lower body condition and fat body volume than nonbrooding and egg-incubating females, and the female condition decreased substantially during parental care. Most mothers and their eggs or offspring were found in close proximity to other nesting females, in high-density nest sites that enhance the potential for social interactions and highlighting the possibility of communal breeding. Parentage was investigated using Amplified Fragment Length Polymorphism (AFLP) genetic markers in 29 offspring from six litters guarded by putative mothers. Our data provide the first evidence of multiple paternity in a caecilian, implying that two fathers sired one litter. Some young from two litters had genotypes not matching the guarding female suggesting that not all offspring are cared for by their biological mothers. This study provides evidence for alloparenting in an amphibian with cost-intensive parental care.

One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona).

Maternal dermatophagy, the eating of maternal skin by offspring, is an unusual form of parental investment involving co-evolved specializations of both maternal skin and offspring dentition, which has been recently discovered in an African caecilian amphibian. Here we report the discovery of this form of parental care in a second, distantly related Neotropical species Siphonops annulatus, where it is characterized by the same syndrome of maternal and offspring specializations. The detailed similarities of skin feeding in different caecilian species provide strong evidence of its homology, implying its presence in the last common ancestor of these species. Biogeographic considerations, the separation of Africa and South American land masses and inferred timescales of amphibian diversification all suggest that skin feeding is an ancient form of parental care in caecilians, which has probably persisted in multiple lineages for more than 100 Myr. These inferences support the hypotheses that (i) maternal dermatophagy is widespread in oviparous direct-developing caecilians, and (ii) that viviparous caecilians that feed on the hypertrophied maternal oviduct evolved from skin-feeding ancestors. In addition to skin-feeding, young S. annulatus were observed to congregate around, and imbibe liquid exuded from, the maternal cloacal opening.

One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona)

Maternal dermatophagy, the eating of maternal skin by offspring, is an unusual form of parental investment involving co-evolved specializations of both maternal skin and offspring dentition, which has been recently discovered in an African caecilian amphibian. Here we report the discovery of this form of parental care in a second, distantly related Neotropical species Siphonops annulatus, where it is characterized by the same syndrome of maternal and offspring specializations. The detailed similarities of skin feeding in different caecilian species provide strong evidence of its homology, implying its presence in the last common ancestor of these species. Biogeographic considerations, the separation of Africa and South American land masses and inferred timescales of amphibian diversification all suggest that skin feeding is an ancient form of parental care in caecilians, which has probably persisted in multiple lineages for more than 100Myr. These inferences support the hypotheses that (i) maternal dermatophagy is widespread in oviparous direct-developing caecilians, and (ii) that viviparous caecilians that feed on the hypertrophied maternal oviduct evolved from skin-feeding ancestors. In addition to skin-feeding, young S. annulatus were observed to congregate around, and imbibe liquid exuded from, the maternal cloacal opening.

Parental investment by skin feeding in a caecilian amphibian.

Although the initial growth and development of most multicellular animals depends on the provision of yolk, there are many varied contrivances by which animals provide additional or alternative investment in their offspring. Providing offspring with additional nutrition should be favoured by natural selection when the consequent increased fitness of the young offsets any corresponding reduction in fecundity. Alternative forms of nutrition may allow parents to delay and potentially redirect their investment. Here we report a remarkable form of parental care and mechanism of parent-offspring nutrient transfer in a caecilian amphibian. Boulengerula taitanus is a direct-developing, oviparous caecilian, the skin of which is transformed in brooding females to provide a rich supply of nutrients for the developing offspring. Young animals are equipped with a specialized dentition, which they use to peel and eat the outer layer of their mother's modified skin. This new form of parental care provides a plausible intermediate stage in the evolution of viviparity in caecilians. At independence, offspring of viviparous and of oviparous dermatotrophic caecilians are relatively large despite being provided with relatively little yolk. The specialized dentition of skin-feeding (dermatophagous) caecilians may constitute a preadaptation to the fetal feeding on the oviduct lining of viviparous caecilians.

Parental investment by skin feeding in a caecilian amphibian

Although the initial growth and development of most multi-cellular animals depends on the provision of yolk, there are many varied contrivances by which animals provide additional or alternative investment in their offspring 1. Providing offspring with additional nutrition should be favoured by natural selection when the consequent increased fitness of the young offsets any corresponding reduction in fecundity2. Alternative forms of nutrition may allow parents to delay and potentially redirect their investment. Here we report a remarkable form of parental care and mechanism of parent-offspring nutrient transfer in a caecilian amphibian. Boulengerula taitanus is a direct-developing, oviparous caecilian3, the skin of which is transformed in brooding females to provide a rich supply of nutrients for the developing offspring. Young animals are equipped with a specialized dentition, which they use to peel and eat the outer layer of their mother's modified skin. This new form of parental care provides a plausible intermediate stage in the evolution of viviparity in caecilians. At independence, offspring of viviparous and of oviparous dermatotrophic caecilians are relatively large despite being provided with relatively little yolk. The specialized dentition of skin-feeding (dermatophagous) caecilians may constitute a pre-adaptation to the fetal feeding on the oviduct lining of viviparous caecilians.