A heterochronic interpretation of the origin of digging adaptations in the northern water vole, Arvicola terrestris (Rodentia: Arvicolidae)

The Palaearctic genus Arvicola includes two species: the south‐western water vole A. sapidus, and the northern water vole A. terrestris. The latter has semiaquatic and/or subterranean populations, while populations of A. sapidus are always semiaquatic. According to the current phylogenetic and palaeontological data, adaptation to semiaquatic life is plesiomorphic for the genus Arvicola. We studied the ontogenetic allometry of skull and long bones of the semiaquatic A. sapidus, a semiaquatic population of A. terrestris (A. t. italicus), and two fossorial populations of A. terrestris (A. t. scherman and A. t. monticola). Animals from fossorial populations were smaller than were those from semiaquatic populations. We found that most of the ontogenetic allometric exponents of characters linked to digging in the skull and in the long bones were significantly higher in A. t. monticola, a fossorial clade, than they were in the semiaquatic populations. On the other hand, there may have been an evolutionary lag between invasion of the hypogeic habitat and the acquisition of fossorial adaptations in A. t. scherman. We showed statistically that the morphological differences linked to the invasion of a hypogeic habitat are already present in juvenile animals and, according to these results, suggest that these morphological differences are the direct expression of genetic changes rather than the outcome of epigenetic factors of mechanical origin. Moreover, we tried to ascertain whether the apomorphic shape of the skull and long bones in the fossorial populations of A. terrestris (compared with the primitive condition that would have been retained by the semiaquatic A. sapidus) are the outcome of a heterochronic process. Optimization by squared change parsimony supported the hypothesis of an apomorphic reduction of body size linked to the invasion of the subterranean habitat. The comparison of the ontogenetic trajectories of both skull shape and long bone shape suggested that a heterochronic process was involved in this morphological transformation. By using the ‘clock model’ method, this mechanism was identified as ‘accelerated dwarfism’ affecting both the skull and long bones. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87 , 381–391.     

Genomic data reveals potential for hybridization,introgression, and incomplete lineage sorting to confound phylogenetic relationships in an adaptive radiation of narrow‐mouth frogs

The microhylid frog genus Kaloula is an adaptive radiation spanning the edge of the Asian mainland and multiple adjacent island archipelagos, with much of the clade's diversity associated with an endemic Philippine radiation. Relationships among clades from the Philippines, however, remain unresolved. With ultraconserved element (UCE) and mitogenomic data, we identified highly supported differences in topology and areas of poor resolution, for each marker set. Using the UCE data, we then identified possible instances of contemporary hybridization, past introgression, and incomplete lineage sorting (ILS) within the Philippine Kaloula. Using a simulation approach, and an estimate of the Philippine Kaloula clade origin (12.7—21.0 mya), we demonstrate that an evolutionary history including inferred instances of hybridization, introgression, and ILS leads to phylogenetic reconstructions that show concordance with results from the observed mitogenome and UCE data. In the process of validating a complex evolutionary scenario in the Philippine Kaloula, we provide the first demonstration of the efficacy of UCE data for phylogenomic studies of anuran amphibians.     

The phylogenetic relationships of the Early Miocene stork Grallavis edwardsi,with comments on the interrelationships of living Ciconiidae (Aves)

The fossil record of storks (Aves, Ciconiidae) includes a relatively large number of specimens from the Middle Eocene onwards, but no taxon is as well represented as Grallavis edwardsi form the Early Miocene of the Allier region in central France. Despite this, the phylogenetic placement of G. edwardsi among other storks has remained elusive not least because of the lack of a robust phylogenetic framework for living storks. To find out how G. edwardsi relates to recent Ciconiidae, we performed a phylogenetic analysis based on osteological features including all living genus‐level taxa of the Ciconiidae. We show that the previously reported similarities to the extant taxa Ephippiorhynchus and Jabiru are based on plesiomorphic features, and our analysis supports a sister group relationship between Grallavis edwardsi and Leptoptilos. Our results are also consistent with a basal divergence within Ciconiidae between Mycteria and Anastomus, which are among the smallest storks, and all other storks. A sister group relationship between storks of the genus Ciconia and all large storks (Leptoptilini) is recovered albeit with weak support, which may be due to homoplastic features linked to their large size. Grallavis edwardsi possessed several osteological adaptations suited for scavenging, and despite lacking some derived traits characteristic of Leptoptilos, it is likely to have been a precursor of large marabou and adjutant storks.     

The evolution of the hallucial tarsometatarsal joint in the Anthropoidea

Changes in the hallucial tarsometatarsal joint, which forms the fulcrum for the grasping hallux, have played a significant role in primate evolution. Comparative studies suggest that one of the morphological novelties heralding the attainment of a monkey grade of structure was the incorporation of the prehallux within this joint. Such a joint is found in the extant Ceboidea and, paradoxically, the Hylobatidae. Hallux and prehallux then form a composite distal articular surface; the proximal surface on the medial cuneiform is completed inferomedially by a convex facet for the prehallux. Divergence of the hallux into the attitude of opposition is accompanied by conjunct rotation, screwing these joint components into a stable, close-packed position. Suppression of the prehallux is accompanied by clear osteological indicators — the absence of prehallux facets on the first metatarsal and medial cuneiform. This modification of the joint is a feature of cercopithecoid evolution, and has also occurred in the hominoid line, after divergence of the ancestral gibbons and apparently after the Dryopithecus (Proconsul) stage. The cladistic relationships indicated by these morphological changes are in striking accord with recent results on primate evolution at the molecular level.     

A multilocus phylogeny of Malagasy scincid lizards elucidates the relationships of the fossorial genera Androngo and Cryptoscincus

A phylogeny for 29 species of scincine lizards from Madagascar, based on 3693 bp of six mitochondrial and five nuclear genes, revealed multiple parallel evolution of adaptations for a burrowing life, and unexpected relationships of the monotypic genera Androngo and Cryptoscincus. Androngo trivittatus was sister to Pygomeles braconnieri, and Cryptoscincus minimus was deeply nested within the genus Paracontias, all of these being fossorial taxa of elongated bodies and partly or fully reduced limbs. To account for these results, we place Cryptoscincus as a junior synonym of Paracontias, and discuss possible taxonomic consequences that may affect the status of Androngo, once additional data become available.     

Do bipolar distributions exist in marine sponges? Stylocordyla chupachups sp. nv. (Porifera: Hadromerida) from the Weddell Sea (Antarctic), previously reported as S. borealis (Lov��n, 1868)

Sponges are the dominant invertebrates in many Antarctic communities, where they play a decisive structural function thanks to their abundance and large sizes. However, current knowledge on Antarctic sponges remains poor even with respect to basic aspects such as taxonomy. Here, we report on an Antarctic species of the genus Stylocordyla, which has been recorded for a long time under the name of the boreal S. borealis due to spicule and growth habit similarities. A thorough study of dense populations of the only Stylocordyla species known up to now from the eastern zone of the Weddell Sea as well as the re-examination of several specimens (including the type material) of S. borealis has allowed us to assess the variability of the boreal species and to confirm that the austral species is not S. borealis (Lovén, 1868) but a new species of Stylocordyla, different from the other congeners recorded from southern latitudes. The new species S. chupachups commonly dwells on horizontal or slighted sloped hard bottoms of the continental shelf of Weddell Sea, from 100 m to below 400 m depth, although the densest populations usually occur between 150 and 300 m. It is a pioneer species in areas that have been scoured by icebergs, and thus its presence may be considered an indicator of recent colonisation.     

Sorting out the Snakebirds: The species status,phylogeny, and biogeography of the Darters (Aves: Anhingidae)

Although the avian family Anhingidae is unequivocally monophyletic, the number and relationships of the component species within the single genus (Anhinga) have long remained unclear. Here, we use extensive mitochondrial and nuclear DNA sequence data (8,878 bp) to show that four species should be recognized. Our fully resolved and well‐supported tree shows that the American Anhinga (Anhinga anhinga) is sister to the three Old World species, with the Oriental (A. melanogaster) and African (A. rufa) Darters sister within the Old World clade, which also includes the Australian Darter (A. novaehollandiae). We estimate that the divergence between the New World and Old World branches occurred 19–22 mya, with the Australian Darter separating from its Old World congeners 14–16 mya and the Oriental and African species splitting ~10 mya. The genus is yet another example of osteological conservatism in the Suliformes, which is comparable to that shown by the cormorants and shags. Nevertheless, the relationships we infer are congruent with recent plumage studies and are biogeographically plausible. We suggest that further investigation of the variation within the African and Australian Darters would be of interest.     

Genetic structure,ecological versatility,and skull shape differentiation in Arvicola water voles (Rodentia,Cricetidae)

Water voles from the genus Arvicola display an amazing ecological versatility, with aquatic and fossorial populations. The Southern water vole (Arvicola sapidus) is largely accepted as a valid species, as well as the newly described Arvicola persicus. In contrast, the taxonomic status and evolutionary relationships within Arvicola amphibiussensu lato had caused a long-standing debate. The phylogenetic relationships among Arvicola were reconstructed using the mitochondrial cytochrome b gene. Four lineages within A. amphibiuss.l. were identified with good support: Western European, Eurasiatic, Italian, and Turkish lineages. Fossorial and aquatic forms were found together in all well-sampled lineages, evidencing that ecotypes do not correspond to distinct species. However, the Western European lineage mostly includes fossorial forms whereas the Eurasiatic lineage tends to include mostly aquatic forms. A morphometric analysis of skull shape evidenced a convergence of aquatic forms of the Eurasiatic lineage toward the typically aquatic shape of A. sapidus. The fossorial form of the Western European lineage, in contrast, displayed morphological adaptation to tooth-digging behavior, with expanded zygomatic arches and proodont incisors. Fossorial Eurasiatic forms displayed intermediate morphologies. This suggests a plastic component of skull shape variation, combined with a genetic component selected by the dominant ecology in each lineage. Integrating genetic distances and other biological data suggest that the Italian lineage may correspond to an incipient species (Arvicola italicus). The three other lineages most probably correspond to phylogeographic variations of a single species (A. amphibius), encompassing the former A. amphibius, Arvicola terrestris, Arvicola scherman, and Arvicola monticola.     

Diversification of African tree frogs (genus Leptopelis) in the highlands of Ethiopia

The frog genus Leptopelis is composed of ~50 species that occur across sub‐Saharan Africa. The majority of these frogs are typically arboreal; however, a few species have evolved a fossorial lifestyle. Most species inhabit lowland forests, but a few species have adapted to high elevations. Five species of Leptopelis occupy the Ethiopian highlands and provide a good opportunity to study the evolutionary transition from an arboreal to a fossorial lifestyle, as well as the diversification in this biodiversity hot spot. We sequenced 14 nuclear and three mitochondrial genes, and generated thousands of SNPs from ddRAD sequencing to study the evolutionary relationships of Ethiopian Leptopelis. The five species of highland Leptopelis form a monophyletic group, which diversified during the late Miocene and Pliocene. We found strong population structure in the fossorial species L. gramineus, with levels of genetic differentiation between populations similar to those found between arboreal species. This could indicate that L. gramineus is a complex of cryptic species. We propose that after the original colonization of the Ethiopian highlands by the ancestor of the L. gramineus group, episodes of vicariance fragmented the ancestral populations of this group. We also report the re‐evolution of arboreality in L. susanae, which evolved from a fossorial ancestor, a rare ecological switch in frogs that had previously been reported only once.     

AN ADAPTIVE RADIATION OF FROGS IN A SOUTHEAST ASIAN ISLAND ARCHIPELAGO

Living amphibians exhibit a diversity of ecologies, life histories, and species‐rich lineages that offers opportunities for studies of adaptive radiation. We characterize a diverse clade of frogs (Kaloula, Microhylidae) in the Philippine island archipelago as an example of an adaptive radiation into three primary habitat specialists or ecotypes. We use a novel phylogenetic estimate for this clade to evaluate the tempo of lineage accumulation and morphological diversification. Because species‐level phylogenetic estimates for Philippine Kaloula are lacking, we employ dense population sampling to determine the appropriate evolutionary lineages for diversification analyses. We explicitly take phylogenetic uncertainty into account when calculating diversification and disparification statistics and fitting models of diversification. Following dispersal to the Philippines from Southeast Asia, Kaloula radiated rapidly into several well‐supported clades. Morphological variation within Kaloula is partly explained by ecotype and accumulated at high levels during this radiation, including within ecotypes. We pinpoint an axis of morphospace related directly to climbing and digging behaviors and find patterns of phenotypic evolution suggestive of ecological opportunity with partitioning into distinct habitat specialists. We conclude by discussing the components of phenotypic diversity that are likely important in amphibian adaptive radiations.     

Life in Burrows Channelled the Morphological Evolution of the Skull in Rodents: the Case of African Mole-Rats (Bathyergidae,Rodentia)

African mole-rats are fossorial rodents that consist of five chisel-tooth digging genera (Heterocephalus, Heliophobius, Georychus, Fukomys, and Cryptomys) and one scratch digger (Bathyergus). They are characterized by striking physiological, morphological, and behavioral adaptations intimately related to their subterranean life. The influence of their mode of life in shaping the cranial morphology has yet to be evaluated in comparison to other Ctenohystrica, especially fossorial genera, which include the subterranean genera Spalacopus and Ctenomys. In our study, we seek to determine to what extent subterranean life affects the morpho-functional properties of the skull among fossorial ctenohystricans. 3D geometric morphometric analyses were performed on 277 skulls, encompassing 63 genera of Ctenohystrica, and complemented by biomechanical studies. African mole-rats and other subterranean Ctenohystrica, especially chisel-tooth diggers, have a short snout, a wide cranium with enlarged zygomatic arches, and a strongly hystricognathous mandible. Even if convergences are also manifest between most fossorial Ctenohystrica, subterranean rodents departed from the main ctenohystrican allometric trends in having a skull shape less size-dependent, but under stronger directional selection with intense digging activity as a major constraint. African mole-rats, notably chisel-tooth diggers, show important mechanical advantage for the temporalis muscles favoring higher forces at the bite point, while mechanical advantage of the superficial masseter muscles is lower compared to other Ctenohystrica. If subterranean species can be clearly discriminated based on their skull morphology, the intrinsic mosaic of anatomical characters of each genus (e.g., skull, teeth, and muscles) can be understood only in the light of their ecology and evolutionary history.     

MOLECULAR PHYLOGENY OF THE GENUS KUMANOA (BATRACHOSPERMALES,RHODOPHYTA)1

Species belonging to the newly established genus Kumanoa were sampled from locations worldwide. DNA sequence data from the rbcL gene, cox1 barcode region, and universal plastid amplicon (UPA) were collected. The new sequence data for the rbcL were combined with the extensive batrachospermalean rbcL data available in GenBank. Single gene rbcL results showed the genus Kumanoa to be a well‐supported clade, and there was high statistical support for many of the terminal nodes. However, with this gene alone, there was very little support for any of the internal nodes. Analysis of the concatenated data set (rbcL, cox1, and UPA) provided higher statistical support across the tree. The taxa K. vittata and K. amazonensis formed a basal grade, and both were on relatively long branches. Three new species are proposed, K. holtonii, K. gudjewga, and K. novaecaledonensis; K. procarpa var. americana is raised to species level. In addition, the synonymy of K. capensis and K. breviarticulata is proposed, with K. capensis having precedence. Five new combinations are made, bringing the total number of accepted species in Kumanoa to 31. The phylogenetic analyses did not reveal any interpretable biogeographic patterns within the genus (e.g., K. spermatiophora from the tropical oceanic island Maui, Hawaii, was sister to K. faroensis from temperate midcontinental Ohio in North America). Previously hypothesized relationships among groups of species were not substantiated in the phylogenetic analyses, and no intrageneric classification is recommended based on current knowledge.     

Tiny steps towards greater knowledge: An osteological review with novel data on the Atlantic Forest toadlets of the Brachycephalus ephippium species group

Brachycephalus is a small, endemic genus of anurans that occur throughout the Brazilian Atlantic Forest. Recent analyses corroborated the monophyly of two species groups within this genus (B. ephippium and B. pernix), whereas the B. didactylus group appears to be polyphyletic. Herein, we compare and describe the skeletal system of all species from the Brachycephalus ephippium species group. We investigated diagnostic characters that are potentially useful to delimit similar species, confirmed the previously proposed genus definition and added six extra characters. We propose an osteological diagnosis for each species of the B. ephippium group, evaluating and describing intraspecific variations. Our results suggest that adults of B. ephippium group have ornamented parotic plates, ornamented post-orbital crests, absence of quadratojugal and neopalatines, distal end of the otic ramus of squamosal expanded towards the parotic plate, reduced zygomatic ramus of the squamosals, posterolateral projection of the crista parotica, presence of ornamented spinal plates (except B. alipioi) and ornamented paravertebral plates. We highlighted the importance of including more than one specimen per species when dealing with miniaturized taxa. A comparison with other Brachycephalus species groups and with Ischnocnema was also provided. Lastly, we suggest some characters to be included in future phylogenetic analysis.     

Phylogenetic analysis of Geotrupidae (Coleoptera, Scarabaeoidea) based on larvae

Abstract. Thirty‐eight characters derived from the larvae of Geotrupidae (Scarabaeoidea, Coleoptera) were analysed using parsimony and Bayesian inference. Trees were rooted with two Trogidae species and one species of Pleocomidae as outgroups. The monophyly of Geotrupidae (including Bolboceratinae) is supported by four autapomorphies: abdominal segments 3–7 with two dorsal annulets, chaetoparia and acanthoparia of the epipharynx not prominent, glossa and hypopharynx fused and without sclerome, trochanter and femur without fossorial setae. Bolboceratinae showed notable differences with Pleocomidae, being more related to Geotrupinae than to other groups. Odonteus species (Bolboceratinae s.str.) appear to constitute the closest sister group to Geotrupinae. Polyphyly of Bolboceratinae is implied by the following apomorphic characters observed in the ‘Odonteus lineage’: anterior and posterior epitormae of epipharynx developed, tormae of epipharynx fused, oncyli of hypopharynx developed, tarsal claws reduced or absent, plectrum and pars stridens of legs well developed and apex of antennal segment 2 with a unique sensorium. A ‘Bolbelasmus lineage’ is supported by the autapomorphic presence of various sensoria on the apex of the antennal segment, and the subtriangular labrum (except Eucanthus). This group constituted by Bolbelasmus, Bolbocerosoma and Eucanthus is the first evidence for a close relationship among genera, but more characters should be analysed to test the support for the clade. A preliminary classification at tribe level of Geotrupinae is suggested as follows: Chromogeotrupini (type genus Chromogeotrupes), Lethrini (type genus Lethrus), Taurocerastini (type genus Taurocerastes) and Geotrupini (type genus Geotrupes). Some ecological facts of Geotrupidae evolution could also be explained by the present results, such as those related to diet and nesting behaviour. Both coprophagy and male–female co‐operation in nesting appear as derived traits.     

Osteological analysis of the killifish genus Cynolebias (Cyprinodontiformes: Rivulidae)

Relationships among the species of the annual fish Cynolebias are unclear. An analysis of the variation and utility of osteological characters for phylogenetic analysis was done using cleared and double-stained specimens representing 21 species of Cynolebias. This analysis showed that some of the characters previously used to diagnose this genus and some of the species are polymorphic. Osteologically, Cynolebias can be diagnosed by the following synapomorphies: (1) triangular-shaped parietal, (2) vomer positioned ventral to the parasphenoid, (3) long ventral process of the dentary, (4) teeth on fourth ceratobranchial, and (5) teeth on first epibranchial. In addition, characters that help define some of the currently recognized species complexes were identified. Species in the “antenori complex” share at least five synapomorphies, such as ossified medial radials of dorsal and anal fins, four pectoral radials, ventral process of the maxillae enlarged, mesopterygoid long relative to the autopalatine, and proportion of cartilage in the basihyal. The “bellottii complex” is characterized by having a reduced basihyal and a deep urohyal, whereas species in the “elongatus complex” possess a caudal fin supported by four vertebrae and have unique modifications of jaw bones. The following osteological features are useful as diagnostic characters at the specific level: (1) Two vertebrae supporting the caudal fin (C. nigripinnis); (2) cartilaginous pelvic bones (C. notatus); (3) short third postcleithrum and broad lateral process of the sphenotic (C. wolterstorffi); (4) thick third postcleithrum (C. gymnoventris); (5) crest on the parietal and reduced in the upper portion of the lacrimal (C. whitei); (6) anteriorly curved lacrimal (C. cheradophilus); (7) second dermosphenotic (C. bellottii); and (8) expansion of the ventral tip of the maxillae and long basyhial (C. constanciae). J. Morphol. 238:245–262, 1998. © 1998 Wiley-Liss, Inc.     

Molecular Phylogeny Supports Repeated Adaptation to Burrowing within Small-Eared Shrews Genus of Cryptotis (Eulipotyphla,Soricidae)

Small-eared shrews of the New World genus Cryptotis (Eulipotyphla, Soricidae) comprise at least 42 species that traditionally have been partitioned among four or more species groups based on morphological characters. The Cryptotis mexicana species group is of particular interest, because its member species inhibit a subtly graded series of forelimb adaptations that appear to correspond to locomotory behaviors that range from more ambulatory to more fossorial. Unfortunately, the evolutionary relationships both among species in the C. mexicana group and among the species groups remain unclear. To better understand the phylogeny of this group of shrews, we sequenced two mitochondrial and two nuclear genes. To help interpret the pattern and direction of morphological changes, we also generated a matrix of morphological characters focused on the evolutionarily plastic humerus. We found significant discordant between the resulting molecular and morphological trees, suggesting considerable convergence in the evolution of the humerus. Our results indicate that adaptations for increased burrowing ability evolved repeatedly within the genus Cryptotis.     

Comparative osteology,relationships, and systematics of fish of the genus <Emphasis Type="Italic">Zoarces</Emphasis> (Zoarcidae,Perciformes)

Comparative-osteological investigation of all species of the genus Zoarces is made: Z. fedorovi, Z. andriashevi, Z. elongatus, Z. viviparus, Z. americanus, and Z. gillii. In the skeleton of hyoid arch in species of Zoarces, Lycozoarces, and Lycodes, paired bony elements are found, not described previously, identified as parurohyalia which may be synapomorphy of Zoarcidae. Differences between the Zoarces species are revealed by 56 external morphological and osteological characters. Cladistic analysis yielded one tree 135, Ci 0.57, Ri 0.54 long. Cladistic analysis confirms validity of a recently described species Z. fedorovi, which turned out to be the most generalized in the genus Zoarces, as well as the validity of Z. elongatus. The species Z. americanus and Z. gillii occupy a terminal position preventing their isolation to independent genera as was previously supposed, as this would lead to paraphyly of the genus Zoarces.