Aurélien Miralles

The integrative future of taxonomy

BackgroundTaxonomy is the biological discipline that identifies, describes, classifies and names extant and extinct species and other taxa. Nowadays, species taxonomy is confronted with the challenge to fully incorporate new theory, methods and data from disciplines that study the origin, limits and evolution of species.ResultsIntegrative taxonomy has been proposed as a framework to bring together these conceptual and methodological developments. Here we review perspectives for an integrative taxonomy that directly bear on what species are, how they can be discovered, and how much diversity is on Earth.ConclusionsWe conclude that taxonomy needs to be pluralistic to improve species discovery and description, and to develop novel protocols to produce the much-needed inventory of life in a reasonable time. To cope with the large number of candidate species revealed by molecular studies of eukaryotes, we propose a classification scheme for those units that will facilitate the subsequent assembly of data sets for the formal description of new species under the Linnaean system, and will ultimately integrate the activities of taxonomists and molecular biologists.

New Metrics for Comparison of Taxonomies Reveal Striking Discrepancies among Species Delimitation Methods in Madascincus Lizards

Delimiting and describing species is fundamental to numerous biological disciplines such as evolution, macroecology, and conservation. Delimiting species as independent evolutionary lineages may and often does yield different outcomes depending on the species criteria applied, but methods should be chosen that minimize the inference of objectively erroneous species limits. Several protocols exploit single-gene or multi-gene coalescence statistics, assignment tests or other rationales related to nuclear DNA (nDNA) allele sharing to automatically delimit species. We apply seven different species delimitation protocols to a taxonomically confusing group of Malagasy lizards (Madascincus), and compare the resulting taxonomies with two newly developed metrics: the Taxonomic index of congruence Ctax which quantifies the congruence between two taxonomies, and the Relative taxonomic resolving power index Rtax which quantifies the potential of an approach to capture a high number of species boundaries. The protocols differed in the total number of species proposed, between 9 and 34, and were also highly incongruent in placing species boundaries. The Generalized Mixed Yule-Coalescent approach captured the highest number of potential species boundaries but many of these were clearly contradicted by extensive nDNA admixture between sympatric mitochondrial DNA (mtDNA) haplotype lineages. Delimiting species as phenotypically diagnosable mtDNA clades failed to detect two cryptic species that are unambiguous due to a lack of nDNA gene flow despite sympatry. We also consider the high number of species boundaries and their placement by multi-gene Bayesian species delimitation as poorly reliable whereas the Bayesian assignment test approach provided a species delimitation highly congruent with integrative taxonomic practice. The present study illustrates the trade-off in taxonomy between reliability (favored by conservative approaches) and resolving power (favored by inflationist approaches). Quantifying excessive splitting is more difficult than quantifying excessive lumping, suggesting a priority for conservative taxonomies in which errors are more liable to be detected and corrected by subsequent studies.

An integrative taxonomic revision of the Cape Verdean skinks (Squamata, Scincidae)

Miralles, A., Vasconcelos, R., Perera, A., Harris, D. J. & Carranza, S. (2010). An integrative taxonomic revision of the Cape Verdean skinks (Squamata, Scincidae). —Zoologica Scripta, 40, 16–44.

Systematics and biogeography of the Neotropical genus Mabuya, with special emphasis on the Amazonian skink Mabuya nigropunctata (Reptilia, Scincidae).

Phylogenetic analyses using up to 1532 base pairs (bp) of mitochondrial DNA from 106 specimens of Neotropical Mabuya, including 18 of the 19 recognized South American and Mesoamerican species, indicate that most species of the genus are monophyletic, including M. nigropunctata that had previously been reported to be paraphyletic. The present results shows that this species includes three highly divergent and largely allopatric lineages restricted to occidental, meridional, and oriental Amazonia. Our dataset demonstrates that previous claims regarding the paraphyletic status of M. nigropunctata and the phylogenetic relationships within this species complex based on the analysis of three mitochondrial and four nuclear genes (approx. 5000bp) were erroneous and resulted from two contaminated cytochrome b sequences. The phylogenetic results indicate that diversification in the Neotropical genus Mabuya started approximately in the Middle Miocene (15.5-13.4Ma). The divergence dates estimated for the Mabuya nigropunctata species complex suggest that the major cladogenetic events that produced the three main groups (occidental (oriental+meridional)) occurred during the Late Miocene. These estimations show that diversification within the M. nigropunctata species complex was not triggered by the climatic changes that occurred during the Pleistocene, as has been suggested by several authors. Rather, our data support the hypothesis that the late tertiary (essentially Miocene epoch) was a period that played a very important role in the generation of biological diversity in the Amazonian forests. Speciation between Mabuyacarvalhoi, endemic to the coastal mountain range of Venezuela, and M. croizati, restricted to the Guiana Shield, occurred during the Middle Miocene and may have been as the result of a vicariant event produced by the formation of the present day Orinoco river drainage basin and the consequent appearance of the Llanos del Orinoco, which acted as a barrier to dispersal between these two species. The split between M. bistriata and M. altamazonica and between the occidental and (meridional+oriental) clades of M. nigropunctata fits very well with the biogeographic split between the eastern and western Amazon basins reported for several other taxa.

Phylogenetic relationships of Trachylepis skink species from Madagascar and the Seychelles (Squamata: Scincidae).

Lizards of the genus Trachylepis are a species-rich group of skinks mainly inhabiting Africa, Madagascar, and several other islands in the western Indian Ocean. All except one probably introduced species of Madagascan Trachylepis are endemic. Two species groups have been distinguished on the basis of subocular scale shape but their phylogenetic relationships remained unclear. We inferred a multilocus phylogeny of the Madagascan Trachylepis species, based on a concatenated dataset of 3261 bp from 3 mitochondrial and 4 nuclear genes with a dense Madagascan taxon sampling and find high support for the monophyly of the endemic Madagascan Trachylepis. The two species groups in Madagascar are highly supported as clades. The highland species T. boettgeri is nested in the T. aureopunctata species group of mainly arid-adapted species, suggesting a colonization of highland swamps by ancestors inhabiting dry western Madagascar. The Seychellois species were sister to the T. maculilabris/T. comorensis clade, suggesting their origin directly out of Africa as with Seychellois chameleons. In Madagascar, a high intraspecific molecular variation was confirmed for T. gravenhorstii, T. elegans, and T. vato, indicating a need for taxonomic revision.

Variations on a bauplan: description of a new Malagasy "mermaid skink" with flipper-like forelimbs only (Scincidae, Sirenoscincus Sakata & Hikida, 2003)

ABSTRACT The “forelimbs only” bauplan, characterised by the combined presence of well-developed fingered forelimbs and the complete absence of hindlimbs, is rare among terrestrial tetrapods. It is restricted to three lineages of squamates with elongated worm-like bodies, the amphisbaenian genus Bipes Lacépède, 1788 and the scincid genera Sirenoscincus Sakata & Hikida, 2003 and Jarujinia Chan-ard, Makchai & Cota, 2011. In the present study, we describe a new species of Sirenoscincus from Marosely, Port Bergé region, northwest Madagascar, which presents a remarkable variation of this bauplan. The forelimbs of S. mobydick n. sp. differ from S. yamagishii Sakata & Hikida, 2003 — the only other known species in the genus — by the complete absence of any fingers or claws, therefore superficially resembling flippers, a combination of characters unique among terrestrial tetrapods. Sirenoscincus mobydick n. sp. is also differentiated from S. yamagishii by several apomorphic cephalic scalation characters, such as: 1) the absence of the frontonasal, likely fused with the frontal (versus presence of both scales); 2) the absence of the preocular, likely fused with the loreal (versus presence of both scales); and 3) the absence of the postsubocular, likely fused with the pretemporal (versus presence of both scales). Additionally, we provide detailed data on the appendicular skeleton of this new species of “mermaid skink” based on X-ray computed tomography that reveal several significant regressions of skeletal elements: 1) autopodial bones highly reduced in size and number; 2) highly reduced pelvic girdle and complete absence of hindlimbs, with the notable exception of two faintly distinguishable bony corpuscles probably representing rudiments of ancestral hindlimb bones; and 3) regressed sclerotic ring with five ossicles only, therefore representing the lowest value ever observed among lizards. Our study highlights the importance of the rare “forelimbs only bauplan” for investigating macroevolutionary questions dealing with complete limb loss in vertebrates, a convergent phenomenon that has repeatedly occurred 16 to 20 times within Scincidae Gray, 1825.

Hypotheses on rostral shield evolution in fossorial lizards derived from the phylogenetic position of a new species of Paracontias (Squamata, Scincidae)

In squamate reptiles the rostral shield constitutes one of the most advanced cases of reduction in the number of scales in the rostral region, an evolutionary trend clearly associated with a burrowing lifestyle. This structure is characterized by the fusion of the rostral scale with all adjacent scales into a large, smooth and conical plate covering the snout, totally encompassing the nostrils, with a horizontal groove running posteriorly from either nostril. In lizards this structure evolved several times independently, in various lineages of limbless skinks and in the family Dibamidae. We performed a multilocus phylogenetic analysis of combined mitochondrial and nuclear DNA sequences from the fossorial genus Paracontias, including P. vermisaurus, a new species described herein under an integrative taxonomic approach. The resulting phylogeny supports monophyly of Paracontias, with the following internal topology: [P. kankana (P. vermisaurus sp. n. (((P. minimus + P. brocchii) (P. manify + P. hildebrandti)) (P. rothschildi + P. fasika)))]. The molecular data, coupled with a comparative morphological study, allows us to investigate the evolution of the snout scales into a single large rostral shield in Paracontias. We discuss the evolutionary processes through which the rostral shield may have originated (e.g. fusion of scales, number and order of steps involved), and conclude that intuitive and apparently obvious hypotheses for scale homologies based on position and size only (as usually formulated in squamate taxonomy) may be highly misleading, even in closely related species. We develop the hypothesis that the rostral shield may provide several functional advantages for fossorial species in facilitating burrowing and protecting the head from strong physical stress, e.g. smoother surface reducing friction between the tegument and the substrate, reduction in the number of flexible sutures resulting in strengthened tegument, and the rostral tip likely playing a role as a shock-absorbing buffer.

Controversial snake relationships supported by reproductive anatomy.

Since the advent of molecular character sets in phylogenetic systematics our understanding of the evolutionary history of snakes has changed considerably. In some cases the novel topologies reconstructed from molecular datasets have left researchers puzzled, as no morphological feature seems to support the new relationships found. This is the case for ‘Amerophidia’sensu Vidal et al. (2007; Biology of the Boas and Pythons, Eagle Mountain: Eagle Mountain Publishing; Aniliidae + Tropidophiidae), a grouping of the Red Pipesnakes and Neotropical Dwarf Boas. We contend that in some cases the apparent lack of historical morphological support for the molecular phylogenies is due to our poor understanding of the organisms as a whole, and not the complete lack of morphological support for controversial clades. For example, we found novel evidence from reproductive anatomy that demonstrates a unique association of the oviducts and cloaca in Amerophidia. Whereas in all other female squamates the oviducts communicate directly with the cloaca, the oviducts of Aniliidae and Tropidophiidae communicate with diverticuli of the cloaca. At present this is the only unambiguous synapomorphy for the Amerophidia. We feel that confirmation of controversial molecular relationships will revolve around the investigation of non‐traditional morphological characters such as reproductive anatomy.

Distinct Patterns of Desynchronized Limb Regression in Malagasy Scincine Lizards (Squamata, Scincidae)

Scincine lizards in Madagascar form an endemic clade of about 60 species exhibiting a variety of ecomorphological adaptations. Several subclades have adapted to burrowing and convergently regressed their limbs and eyes, resulting in a variety of partial and completely limbless morphologies among extant taxa. However, patterns of limb regression in these taxa have not been studied in detail. Here we fill this gap in knowledge by providing a phylogenetic analysis of DNA sequences of three mitochondrial and four nuclear gene fragments in an extended sampling of Malagasy skinks, and microtomographic analyses of osteology of various burrowing taxa adapted to sand substrate. Based on our data we propose to (i) consider Sirenoscincus Sakata & Hikida, 2003, as junior synonym of Voeltzkowia Boettger, 1893; (ii) resurrect the genus name Grandidierina Mocquard, 1894, for four species previously included in Voeltzkowia; and (iii) consider Androngo Brygoo, 1982, as junior synonym of Pygomeles Grandidier, 1867. By supporting the clade consisting of the limbless Voeltzkowia mira and the forelimb-only taxa V. mobydick and V. yamagishii, our data indicate that full regression of limbs and eyes occurred in parallel twice in the genus Voeltzkowia (as hitherto defined) that we consider as a sand-swimming ecomorph: in the Voeltzkowia clade sensu stricto the regression first affected the hindlimbs and subsequently the forelimbs, whereas the Grandidierina clade first regressed the forelimbs and subsequently the hindlimbs following the pattern prevalent in squamates. Timetree reconstructions for the Malagasy Scincidae contain a substantial amount of uncertainty due to the absence of suitable primary fossil calibrations. However, our preliminary reconstructions suggest rapid limb regression in Malagasy scincids with an estimated maximal duration of 6 MYr for a complete regression in Paracontias, and 4 and 8 MYr respectively for complete regression of forelimbs in Grandidierina and hindlimbs in Voeltzkowia.

Molecular phylogenetics and biogeography of the Neotropical skink genus Mabuya Fitzinger (Squamata: Scincidae) with emphasis on Colombian populations ☆

Understanding the phylogenetic and geographical history of Neotropical lineages requires having adequate geographic and taxonomic sampling across the region. However, Colombia has remained a geographical gap in many studies of Neotropical diversity. Here we present a study of Neotropical skinks of the genus Mabuya, reptiles that are difficult to identify or delimit due to their conservative morphology. The goal of the present study is to propose phylogenetic and biogeographic hypotheses of Mabuya including samples from the previously under-studied territory of Colombia, and address relevant biogeographic and taxonomic issues. We combined molecular and morphological data sampled densely by us within Colombia with published data representing broad sampling across the Neotropical realm, including DNA sequence data from two mitochondrial (12S rRNA and cytochrome b) and three nuclear genes (Rag2, NGFB and R35). To evaluate species boundaries we employed a general mixed Yule-coalescent (GMYC) model applied to the mitochondrial data set. Our results suggest that the diversity of Mabuya within Colombia is higher than previously recognized, and includes lineages from Central America and from eastern and southern South America. The genus appears to have originated in eastern South America in the Early Miocene, with subsequent expansions into Central America and the Caribbean in the Late Miocene, including at least six oceanic dispersal events to Caribbean Islands. We identified at least four new candidate species for Colombia and two species that were not previously reported in Colombia. The populations of northeastern Colombia can be assigned to M. zuliae, while specimens from Orinoquia and the eastern foothills of the Cordillera Oriental of Colombia correspond to M. altamazonica. The validity of seven species of Mabuya sensu lato was not supported due to a combination of three factors: (1) non-monophyly, (2) <75% likelihood bootstrap support and <0.95 Bayesian posterior probability, and (3) GMYC analysis collapsing named species. Finally, we suggest that Mabuya sensu stricto may be regarded as a diverse monophyletic genus, widely distributed throughout the Neotropics.