Theory predicts that sexually dimorphic traits under strong sexual selection, particularly those involved with intersexual signaling, can accelerate speciation and produce bursts of diversification. ...Sexual dichromatism (sexual dimorphism in color) is widely used as a proxy for sexual selection and is associated with rapid diversification in several animal groups, yet studies using phylogenetic comparative methods to explicitly test for an association between sexual dichromatism and diversification have produced conflicting results. Sexual dichromatism is rare in frogs, but it is both striking and prevalent in African reed frogs, a major component of the diverse frog radiation termed Afrobatrachia. In contrast to most other vertebrates, reed frogs display female-biased dichromatism in which females undergo color transformation, often resulting in more ornate coloration in females than in males. We produce a robust phylogeny of Afrobatrachia to investigate the evolutionary origins of sexual dichromatism in this radiation and examine whether the presence of dichromatism is associated with increased rates of net diversification. We find that sexual dichromatism evolved once within hyperoliids and was followed by numerous independent reversals to monochromatism. We detect significant diversification rate heterogeneity in Afrobatrachia and find that sexually dichromatic lineages have double the average net diversification rate of monochromatic lineages. By conducting trait simulations on our empirical phylogeny, we demonstrate that our inference of trait-dependent diversification is robust. Although sexual dichromatism in hyperoliid frogs is linked to their rapid diversification and supports macroevolutionary predictions of speciation by sexual selection, the function of dichromatism in reed frogs remains unclear. We propose that reed frogs are a compelling system for studying the roles of natural and sexual selection on the evolution of sexual dichromatism across micro- and macroevolutionary timescales.
Our current understanding of vertebrate skin and gut microbiomes, and their vertical transmission, remains incomplete as major lineages and varied forms of parental care remain unexplored. The ...diverse and elaborate forms of parental care exhibited by amphibians constitute an ideal system to study microbe transmission, yet investigations of vertical transmission among frogs and salamanders have been inconclusive. In this study, we assess bacteria transmission in Herpele squalostoma, an oviparous direct-developing caecilian in which females obligately attend juveniles that feed on their mother's skin (dermatophagy).
We used 16S rRNA amplicon-sequencing of the skin and gut of wild caught H. squalostoma individuals (males, females, including those attending juveniles) as well as environmental samples. Sourcetracker analyses revealed that juveniles obtain an important portion of their skin and gut bacteria communities from their mother. The contribution of a mother's skin to the skin and gut of her respective juveniles was much larger than that of any other bacteria source. In contrast to males and females not attending juveniles, only the skins of juveniles and their mothers were colonized by bacteria taxa Verrucomicrobiaceae, Nocardioidaceae, and Erysipelotrichaceae. In addition to providing indirect evidence for microbiome transmission linked to parental care among amphibians, our study also points to noticeable differences between the skin and gut communities of H. squalostoma and that of many frogs and salamanders, which warrants further investigation.
Our study is the first to find strong support for vertical bacteria transmission attributed to parental care in a direct-developing amphibian species. This suggests that obligate parental care may promote microbiome transmission in caecilians.
Secondary sympatry amongst sister lineages is strongly associated with genetic and ecological divergence. This pattern suggests that for closely related species to coexist in secondary sympatry, they ...must accumulate differences in traits that mediate ecological and/or reproductive isolation. Here, we characterized inter‐ and intraspecific divergence in three giant tree frog species whose distributions stretch across West and Central Africa. Using genome‐wide single‐nucleotide polymorphism data, we demonstrated that species‐level divergence coincides temporally and geographically with a period of large‐scale forest fragmentation during the late Pliocene. Our environmental niche models further supported a dynamic history of climatic suitability and stability, and indicated that all three species occupy distinct environmental niches. We found modest morphological differentiation amongst the species with significant divergence in tympanum diameter and male advertisement call. In addition, we confirmed that two species occur in secondary sympatry in Central Africa but found no evidence of hybridization. These patterns support the hypothesis that cycles of genetic exchange and isolation across West and Central Africa have contributed to globally significant biodiversity. Furthermore, divergence in both ecology and reproductive traits appear to have played important roles in maintaining distinct lineages. At the intraspecific level, we found that climatic refugia, precipitation gradients, marine incursions, and potentially riverine barriers generated phylogeographic structure throughout the Pleistocene and into the Holocene. Further studies examining phenotypic divergence and secondary contact amongst these geographically structured populations may demonstrate how smaller scale and more recent biogeographic barriers contribute to regional diversification.
La sympatrie secondaire parmi les espèces sœurs est fortement associée à la divergence génétique et écologique. Ce modèle suggère que pour que des espèces étroitement liées coexistent en sympatrie secondaire, elles doivent accumuler des différences dans les traits qui contribuent à l'isolement écologique ou reproductif. Ici, nous avons caractérisé la divergence inter‐ et intra‐spécifique chez trois espèces de grenouilles arboricoles géantes dont les distributions s'étendent à travers l'Afrique de l'Ouest et Centrale. Avec des données génétiques, nous avons démontré que la divergence au niveau des espèces coïncide temporellement et géographiquement avec une période de fragmentation forestière à la fin du Pliocène. Nos modèles de niches environnementales ont soutenu une histoire dynamique de stabilité climatique, et ont indiqué que les trois espèces occupent des niches environnementales distinctes. Nous avons trouvé une différenciation morphologique modeste parmi les trois espèces mais une divergence significative dans le diamètre du tympan et les cris des mâles. De plus, nous avons confirmé que deux espèces sont présentes en sympatrie secondaire en Afrique Centrale mais n'avons trouvé aucune preuve d'hybridation. Ces résultats soutiennent l'hypothèse que les cycles d'échange génétique et d'isolement à travers l'Afrique de l'Ouest et Centrale ont contribué à une profonde concentration de biodiversité dans la région. De plus, la divergence des traits écologiques et reproducteurs semble avoir joué un rôle important dans le maintien de lignées distinctes. Au niveau intra‐spécifique, nous avons constaté que les refuges climatiques, les gradients de précipitation, les incursions marines et potentiellement les barrières fluviales ont généré une structure phylogéographique pendant le Pléistocène et jusqu'à l'Holocène. Des études examinant la divergence phénotypique et le contact secondaire entre ces populations géographiquement structurées pourraient démontrer comment des barrières biogéographiques à échelle plus petite et plus récentes contribuent à la diversification régionale.
see also the Perspective by Bryan C. Carstens and Shelby P. Moshier
Introduction
Emerging infectious diseases are increasingly recognized as a global threat to wildlife. Pandemics in amphibians, caused by the fungal pathogen
Batrachochytrium dendrobatidis
(
Bd
), ...have resulted in biodiversity loss at a global scale. Genomic data suggest a complex evolutionary history of
Bd
lineages that vary in pathogenicity. Africa harbors a significant proportion of global amphibian biodiversity, and multiple
Bd
lineages are known to occur there; yet, despite the decline of many host species, there are currently no described
Bd
-epizootics. Here, we describe the historical and recent biogeographical spread of
Bd
and assess its risk to amphibians across the continent of Africa.
Methods
We provide a 165-year view of host-pathogen interactions by (i) employing a
Bd
assay to test 4,623 specimens (collected 1908–2013); (ii) compiling 12,297 published
Bd
records (collected 1852–2017); (iii) comparing the frequency of
Bd
-infected amphibians through time by both country and region; (iv) genotyping
Bd
lineages; (v) histologically identifying evidence of chytridiomycosis, and (vi) using a habitat suitability model to assess future
Bd
risk.
Results
We found a pattern of
Bd
emergence beginning largely at the turn of the century. From 1852–1999, we found low
Bd
prevalence (3.2% overall) and limited geographic spread, but after 2000 we documented a sharp increase in prevalence (18.7% overall), wider geographic spread, and multiple
Bd
lineages that may be responsible for emergence in different regions. We found that
Bd
risk to amphibians was highest in much of eastern, central, and western Africa.
Discussion
Our study documents a largely overlooked yet significant increase in a fungal pathogen that could pose a threat to amphibians across an entire continent. We emphasize the need to bridge historical and contemporary datasets to better describe and predict host-pathogen dynamics over larger temporal scales.
Batrachochytrium dendrobatidis (Bd) is commonly termed the ‘amphibian chytrid fungus’ but thus far has been documented to be a pathogen of only batrachian amphibians (anurans and caudatans). It is ...not proven to infect the limbless, generally poorly known, and mostly soil-dwelling caecilians (Gymnophiona). We conducted the largest qPCR survey of Bd in caecilians to date, for more than 200 field-swabbed specimens from five countries in Africa and South America, representing nearly 20 species, 12 genera, and 8 families. Positive results were recovered for 58 specimens from Tanzania and Cameroon (4 families, 6 genera, 6+ species). Quantities of Bd were not exceptionally high, with genomic equivalent (GE) values of 0.052–17.339. In addition, we report the first evidence of lethal chytridiomycosis in caecilians. Mortality in captive (wild-caught, commercial pet trade) Geotrypetes seraphini was associated with GE scores similar to those we detected for field-swabbed, wild animals.
The indotyphlid caecilian amphibian Idiocranium russeli Parker, 1936 is the only nominal species in its genus. Apart from two additional, largely overlooked locality records that we consider to be of ...an undescribed species, I. russeli is known with certainty from only a single collection of c .50 specimens from a single locality in 1933. We report new material from fieldwork in 2012 carried out in the vicinity of the type locality. Digging surveys at 34 sites for a total of >2000 person minutes found 50 I. russeli at 15 of these sites, extending the known range of the species by more than 40 km south and from an elevation of c .670 m to 104–820 m. The species probably occurs in nearby Nigeria and in some protected areas, is tolerant of some human disturbance, and is likely to move from Data Deficient to Least Concern on the IUCN Red List. Males have relatively longer and wider heads than females. Total length measured for preserved specimens is less than for freshly anaesthetized specimens, by up to 14.1%. Previously, preserved I. russeli were reported as having a maximum length of 114 mm, but the new sample includes specimens with total lengths of 145 mm in preservation and 167 mm when fresh. The sex of the smallest independent specimens (total length 62 mm in preservation) could be determined from examination of the gonads, hatchlings are c.30 mm, and I. russeli is confirmed as one of the smallest known caecilian species.
An adult (presumably female) Herpele squalostoma was found attending 16 young in Cameroon. Four young that were preserved one day after collection have multicusped teeth and skin-like material in ...their gut. The adult and remaining young were maintained in captivity without provision of food for one month. During this period the young gained more than 10% in mass. Twenty-nine days after collection one additional young was preserved, this has adult-like dentition. We conclude that H. squalostoma resembles the oviparous caecilians Boulengerula taitanus and Siphonops annulatus in having young that receive extended parental care and that remove and eat the stratum corneum of maternal skin using specialized deciduous teeth. This discovery matches a prediction that maternal dermatophagy is widespread (and homologous) among teresomatan caecilians.
An adult (presumably female) Herpele squalostomawas found attending 16 young in Cameroon. Four young that were preserved one day after collection have multicusped teeth and skin-like material in ...their gut. The adult and remaining young were maintained in captivity without provision of food for one month. During this period the young gained more than 10% in mass. Twenty-nine days after collection one additional young was preserved, this has adult-like dentition. We conclude that H. squalostomaresembles the oviparous caecilians Boulengerula taitanusand Siphonops annulatusin having young that receive extended parental care and that remove and eat the stratum corneum of maternal skin using specialized deciduous teeth. This discovery matches a prediction that maternal dermatophagy is widespread (and homologous) among teresomatan caecilians. PUBLICATION ABSTRACT
Aim: To investigate how putative barriers, forest refugia, and ecological gradients across the lower Guineo-Congolian rain forest shape genetic and phenotypic divergence in the leaf-folding frog ...Afrixalus paradorsalis, and examine the role of adjacent land bridge and sky-islands in diversification. Location: The Lower Guineo-Congolian Forest, the Cameroonian Volcanic Line (CVL), and Bioko Island, Central Africa. Taxon: Afrixalus paradorsalis (Family: Hyperoliidae), an African leaf-folding frog. Methods: We used molecular and phenotypic data to investigate diversity and divergence among the A. paradorsalis species complex distributed across lowland rain forests, a land bridge island, and mountains in Central Africa. We examined the coincidence of population boundaries, landscape features, divergence times, and spatial patterns of connectivity and diversity, and subsequently performed demographic modelling using genome-wide SNP variation to distinguish among divergence mechanisms in mainland (riverine barriers, forest refugia, ecological gradients) and land bridge island populations (vicariance, Overwater dispersal). Results: We detected four genetically distinct allopatric populations corresponding to Bioko Island, the CVL, and two lowland rain forest populations split by the Sanaga River. Although lowland populations are phenotypically indistinguishable, pronounced body size evolution occurs at high elevation, and the timing of the formation of the high elevation population coincides with mountain uplift in the CVL. Spatial analyses and demographic modelling revealed population divergence across mainland Lower Guinea is best explained by forest refugia rather than riverine barriers or ecological gradients, and that the Bioko Island population divergence is best explained by vicariance (marine incursion) rather than overseas dispersal. Main conclusions: We provide growing support for the important role of forest refugia in driving intraspecific divergences in the Guineo-Congolian rain forest. In A. paradorsalis, sky-islands in the CVL have resulted in greater genetic and phenotypic divergences than marine incursions of the land bridge Bioko Island, highlighting important differences in patterns of island-driven diversification in Lower Guinea.
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