Emma Sherratt

Discovery of a new family of amphibians from northeast India with ancient links to Africa

The limbless, primarily soil-dwelling and tropical caecilian amphibians (Gymnophiona) comprise the least known order of tetrapods. On the basis of unprecedented extensive fieldwork, we report the discovery of a previously overlooked, ancient lineage and radiation of caecilians from threatened habitats in the underexplored states of northeast India. Molecular phylogenetic analyses of mitogenomic and nuclear DNA sequences, and comparative cranial anatomy indicate an unexpected sister-group relationship with the exclusively African family Herpelidae. Relaxed molecular clock analyses indicate that these lineages diverged in the Early Cretaceous, about 140 Ma. The discovery adds a major branch to the amphibian tree of life and sheds light on both the evolution and biogeography of caecilians and the biotic history of northeast India—an area generally interpreted as a gateway between biodiversity hotspots rather than a distinct biogeographic unit with its own ancient endemics. Because of its distinctive morphology, inferred age and phylogenetic relationships, we recognize the newly discovered caecilian radiation as a new family of modern amphibians.

A search for quantitative trait loci exhibiting imprinting effects on mouse mandible size and shape

Genomic imprinting refers to the pattern of monoallelic parent-of-origin-dependent gene expression where one of the two alleles at a locus is expressed and the other silenced. Although some genes in mice are known to be imprinted, the true scope of imprinting and its impact on the genetic architecture of a wide range of morphometric traits is mostly unknown. We therefore searched for quantitative trait loci (QTL) exhibiting imprinting effects on mandible size and shape traits in a large F3 population of mice originating from an intercross of the LG/J (Large) and SM/J (Small) inbred strains. We discovered a total of 51 QTL affecting mandible size and shape, 6 of which exhibited differences between reciprocal heterozygotes, the usual signature of imprinting effects. However, our analysis showed that only one of these QTL (affecting mandible size) exhibited a pattern consistent with true imprinting effects, whereas reciprocal heterozygote differences in the other five all were due to maternal genetic effects. We concluded that genomic imprinting has a negligible effect on these specific morphometric traits, and that maternal genetic effects may account for many of the previously reported instances of apparent genomic imprinting.

A relative shift in cloacal location repositions external genitalia in amniote evolution

The move of vertebrates to a terrestrial lifestyle required major adaptations in their locomotory apparatus and reproductive organs. While the fin-to-limb transition has received considerable attention, little is known about the developmental and evolutionary origins of external genitalia. Similarities in gene expression have been interpreted as a potential evolutionary link between the limb and genitals; however, no underlying developmental mechanism has been identified. We re-examined this question using micro-computed tomography, lineage tracing in three amniote clades, and RNA-sequencing-based transcriptional profiling. Here we show that the developmental origin of external genitalia has shifted through evolution, and in some taxa limbs and genitals share a common primordium. In squamates, the genitalia develop directly from the budding hindlimbs, or the remnants thereof, whereas in mice the genital tubercle originates from the ventral and tail bud mesenchyme. The recruitment of different cell populations for genital outgrowth follows a change in the relative position of the cloaca, the genitalia organizing centre. Ectopic grafting of the cloaca demonstrates the conserved ability of different mesenchymal cells to respond to these genitalia-inducing signals. Our results support a limb-like developmental origin of external genitalia as the ancestral condition. Moreover, they suggest that a change in the relative position of the cloacal signalling centre during evolution has led to an altered developmental route for external genitalia in mammals, while preserving parts of the ancestral limb molecular circuitry owing to a common evolutionary origin.

CONVERGENT EVOLUTION OF SEXUAL DIMORPHISM IN SKULL SHAPE USING DISTINCT DEVELOPMENTAL STRATEGIES

Studies integrating evolutionary and developmental analyses of morphological variation are of growing interest to biologists as they promise to shed fresh light on the mechanisms of morphological diversification. Sexually dimorphic traits tend to be incredibly divergent across taxa. Such diversification must arise through evolutionary modifications to sex differences during development. Nevertheless, few studies of dimorphism have attempted to synthesize evolutionary and developmental perspectives. Using geometric morphometric analysis of head shape for 50 Anolis species, we show that two clades have converged on extreme levels of sexual dimorphism through similar, male‐specific changes in facial morphology. In both clades, males have evolved highly elongate faces whereas females retain faces of more moderate proportion. This convergence is accomplished using distinct developmental mechanisms; one clade evolved extreme dimorphism through the exaggeration of a widely shared, potentially ancestral, developmental strategy whereas the other clade evolved a novel developmental strategy not observed elsewhere in the genus. Together, our analyses indicate that both shared and derived features of development contribute to macroevolutionary patterns of morphological diversity among Anolis lizards.

Amphibian diversity in East African biodiversity hotspots: altitudinal and latitudinal patterns

The Eastern Arc mountain chain and adjoining coastal forests of Tanzania and Kenya have been listed as world biodiversity hotspots. We report on an ongoing attempt to estimate amphibian diversity on the three best studied mountains of the Eastern Arc, the East Usambara, Uluguru and Udzungwa mountains of Tanzania, complemented by an estimate of diversity on the adjoining coastal lowland. This proves to be a complex task, which introduces a note of caution into evaluating global biodiversity estimates. Most amphibian species in eastern Tanzania occur on the coastal lowlands and are widely distributed, extending at least north or south of Tanzania and, to a variable extent, westwards to the elevated interior. Diversity patterns along the length of the lowlands are complex, with the presence of a Sahelian element in the extreme north. On the three Eastern Arc mountains studied, species turnover associated with rising altitude is greater than turnover associated with latitudinal distance between the mountain blocks, leading to greater altitudinal than latitudinal diversity in this equatorial region. A long-standing divergence is indicated between montane and lowland endemics. Although forest-associated species are not the largest contributor to the eastern Tanzanian total species diversity (some 48%), the uniqueness of these species both in lowland and montane forests, combined with their evident vulnerability to disturbance, makes them a subject for particular conservation concern, and justifies hotspot status for both montane and lowland forests.

Evolution of Cranial Shape in Caecilians (Amphibia: Gymnophiona)

Insights into morphological diversification can be obtained from the ways the species of a clade occupy morphospace. Projecting a phylogeny into morphospace provides estimates of evolutionary trajectories as lineages diversified information that can be used to infer the dynamics of evolutionary processes that produced patterns of morphospace occupation. We present here a large-scale investigation into evolution of morphological variation in the skull of caecilian amphibians, a major clade of vertebrates. Because caecilians are limbless, predominantly fossorial animals, diversification of their skull has occurred within a framework imposed by the functional demands of head-first burrowing. We examined cranial shape in 141 species, over half of known species, using X-ray computed tomography and geometric morphometrics. Mapping an existing phylogeny into the cranial morphospace to estimate the history of morphological change (phylomorphospace), we find a striking pattern: most species occupy distinct clusters in cranial morphospace that closely correspond to the main caecilian clades, and each cluster is separated by unoccupied morphospace. The empty spaces in shape space are unlikely to be caused entirely by extinction or incomplete sampling. The main caecilian clades have different amounts of morphological disparity, but neither clade age nor number of species account for this variation. Cranial shape variation is clearly linked to phyletic divergence, but there is also homoplasy, which is attributed to extrinsic factors associated with head-first digging: features of caecilian crania that have been previously argued to correlate with differential microhabitat use and burrowing ability, such as subterminal and terminal mouths, degree of temporal fenestration (stegokrotaphy/zygokrotaphy), and eyes covered by bone, have evolved and many combinations occur in modern species. We find evidence of morphological convergence in cranial shape, among species that have eyes covered by bone, resulting in a narrow bullet-shaped head. These results reveal a complex history, including early expansion of morphospace and both divergent and convergent evolution resulting in the diversity we observe today.

A New Species of Skin-Feeding Caecilian and the First Report of Reproductive Mode in Microcaecilia (Amphibia: Gymnophiona: Siphonopidae)

A new species of siphonopid caecilian, Microcaecilia dermatophaga sp. nov., is described based on nine specimens from French Guiana. The new species is the first new caecilian to be described from French Guiana for more than 150 years. It differs from all other Microcaecilia in having fewer secondary annular grooves and/or in lacking a transverse groove on the dorsum of the first collar. Observations of oviparity and of extended parental care in M. dermatophaga are the first reproductive mode data for any species of the genus. Microcaecilia dermatophaga is the third species, and represents the third genus, for which there has been direct observation of young animals feeding on the skin of their attending mother. The species is named for this maternal dermatophagy, which is hypothesised to be characteristic of the Siphonopidae.

Amber fossils demonstrate deep-time stability of Caribbean lizard communities

Significance An unresolved question in ecology is whether the structure of ecological communities can be stable over very long timescales. Here we describe a wealth of new amber fossils for an ancient radiation of Hispaniolan lizards that, until now, has had a very poor fossil record. These fossils provide an important and previously unavailable perspective on an ecologically well-studied group and indicate that anole lizard communities occurring on Hispaniola 20 Mya were made up of the same types of habitat specialists present in this group today. These data indicate that the ecological processes important in extant anole communities have been operative over long periods of time. Whether the structure of ecological communities can exhibit stability over macroevolutionary timescales has long been debated. The similarity of independently evolved Anolis lizard communities on environmentally similar Greater Antillean islands supports the notion that community evolution is deterministic. However, a dearth of Caribbean Anolis fossils—only three have been described to date—has precluded direct investigation of the stability of anole communities through time. Here we report on an additional 17 fossil anoles in Dominican amber dating to 15–20 My before the present. Using data collected primarily by X-ray microcomputed tomography (X-ray micro-CT), we demonstrate that the main elements of Hispaniolan anole ecomorphological diversity were in place in the Miocene. Phylogenetic analysis yields results consistent with the hypothesis that the ecomorphs that evolved in the Miocene are members of the same ecomorph clades extant today. The primary axes of ecomorphological diversity in the Hispaniolan anole fauna appear to have changed little between the Miocene and the present, providing evidence for the stability of ecological communities over macroevolutionary timescales.

Trends in the sand: directional evolution in the shell shape of recessing scallops (Bivalvia: Pectinidae)

Directional evolution is one of the most compelling evolutionary patterns observed in macroevolution. Yet, despite its importance, detecting such trends in multivariate data remains a challenge. In this study, we evaluate multivariate evolution of shell shape in 93 bivalved scallop species, combining geometric morphometrics and phylogenetic comparative methods. Phylomorphospace visualization described the history of morphological diversification in the group; revealing that taxa with a recessing life habit were the most distinctive in shell shape, and appeared to display a directional trend. To evaluate this hypothesis empirically, we extended existing methods by characterizing the mean directional evolution in phylomorphospace for recessing scallops. We then compared this pattern to what was expected under several alternative evolutionary scenarios using phylogenetic simulations. The observed pattern did not fall within the distribution obtained under multivariate Brownian motion, enabling us to reject this evolutionary scenario. By contrast, the observed pattern was more similar to, and fell within, the distribution obtained from simulations using Brownian motion combined with a directional trend. Thus, the observed data are consistent with a pattern of directional evolution for this lineage of recessing scallops. We discuss this putative directional evolutionary trend in terms of its potential adaptive role in exploiting novel habitats.

Influence of fossoriality on inner ear morphology: insights from caecilian amphibians

It is widely accepted that a relationship exists between inner ear morphology and functional aspects of an animals biology, such as locomotor behaviour. Animals that engage in agile and spatially complex behaviours possess semicircular canals that morphologically maximise sensitivity to correspondingly complex physical stimuli. Stemming from the prediction that fossorial tetrapods require a well‐developed sense of spatial awareness, we investigate the hypothesis that fossoriality leads to inner ear morphology that is convergent with other spatially adept tetrapods. We apply morphometrics to otic capsule endocasts of 26 caecilian species to quantify aspects of inner ear shape, and compare these with a sample of frog and salamander species. Our results reveal caecilians (and also frogs) possess strongly curved canals, a feature in common with spatially adept species. However, significantly shorter canals in caecilians suggest reduced sensitivity, possibly associated with reduced reliance on vestibulo‐ocular reflexes in this group of visually degenerate tetrapods. An elaboration of the sacculus of caecilians is interpreted as a unique adaptation among amphibians to increase sensitivity to substrate‐borne vibrations transmitted through the head. This study represents the first quantitative analyses of inner ear morphology of limbless fossorial tetrapods, and identifies features within a new behavioural context that will contribute to our understanding of the biological consequences of physical stimuli on sensory function and associated morphological evolution.