Systematic revision of Brachypelma red-kneed tarantulas (Araneae:Theraphosidae), and the use of DNA barcodes to assist in the identification and conservation of CITES-listed species.
Invertebrate Systematics 31(2):157-179. DOI:10.1071/IS16023
Mexican red-kneed tarantulas of the genus Brachypelma are regarded as some of the most desirable invertebrate pets, and although bred in captivity, they continue to be smuggled out of the wild in large numbers. Species are often difficult to identify based solely on morphology, therefore prompt and accurate identification is required for adequate protection. Thus, we explored the applicability of using COI-based DNA barcoding as a complementary identification tool. Brachypelma smithi (F. O. Pickard-Cambridge, 1897) and Brachypelma hamorii Tesmongt, Cleton & Verdez, 1997 are redescribed, and their morphological differences defined. Brachypelma annitha is proposed as a new synonym of B. smithi. The current distribution of red-kneed tarantulas shows that the Balsas River basin may act as a geographical barrier. Morphological and molecular evidence are concordant and together provide robust hypotheses for delimiting Mexican red-kneed tarantula species. DNA barcoding of these tarantulas is further shown to be useful for species-level identification and for potentially preventing black market trade in these spiders. As a Convention on International Trade in Endangered Species (CITES) listing does not protect habitat, or control wildlife management or human interactions with organisms, it is important to support environmental conservation activities to provide an alternative income for local communities and to avoid damage to wildlife populations.
Generic Revision in the Holarctic Ground Squirrel Genus Spermophilus.
Journal of Mammalogy 90 (2), 14 April 2009, Pages 270–305, https://doi.org/10.1644/07-MAMM-A-309.1
The substantial body of research on Holarctic ground squirrels amassed over the past century documents considerable variability in morphological, cytogenetic, ecological, and behavioral attributes in the genus Spermophilus F. Cuvier, 1825. Recent molecular phylogenetic studies suggest that the traditionally recognized genera Marmota Blumenbach, 1779 (marmots), Cynomys Rafinesque, 1817 (prairie dogs), and Ammospermophilus Merriam, 1892 (antelope ground squirrels) render Spermophilus paraphyletic, potentially suggesting that multiple generic-level lineages should be credited within Spermophilus. Herein, we recognize 8 genera formerly subsumed in Spermophilus, each of which is morphologically diagnosable, craniometrically distinctive, and recovered as a monophyletic clade in phylogenetic analyses utilizing the mitochondrial gene cytochrome b. Generic-level names are available for each of these ground squirrel assemblages, most of which are exclusively or predominantly North American in distribution (Notocitellus A. H. Howell, 1938; Otospermophilus Brandt, 1844; Callospermophilus Merriam, 1897; Ictidomys J. A. Allen, 1877; Poliocitellus A. H. Howell, 1938; Xerospermophilus Merriam, 1892; and Urocitellus Obolenskij, 1927). Only Spermophilus sensu stricto is restricted to Eurasia. Generic subdivision of Spermophilus more aptly illuminates the taxonomic relationships, ecomorphological disparity, and biogeographic history of Holarctic ground squirrels.
Multivariate species boundaries and conservation of harlequin poison frogs.
Molecular Ecology 27 (17): 3432-3451.
In this study, we present an iterative method for delimiting species under the general lineage concept (GLC) based on the multivariate clustering of morphological, ecological and genetic data. Our rationale is that distinct multivariate groups correspond to evolutionarily independent metapopulation lineages because they reflect the common signal of different secondary defining properties (environmental and genetic distinctiveness, phenotypic diagnosability, etc.) that imply the existence of barriers preventing or limiting gene exchange. We applied this method to study a group of endangered poison frogs, the Oophaga histrionica complex. In our study case, we used next-generation targeted amplicon sequencing to obtain a robust genetic data set that we combined with patterns of morphological and ecological features. Our analyses revealed the existence of at least five different species in the histrionica complex (three, new to science), some of them, occurring in small isolated populations outside any protected areas. The lineage delimitation proposed here has important conservation implications as it revealed that some of the Oophaga species should be considered among the most vulnerable of the Neotropical frogs. More broadly, our study exemplifies how multiple-amplicon and multivariate statistical techniques can be integrated to successfully identify species and their boundaries.
A Taxonomic Reassessment of Cacajao melanocephalus Humboldt (1811), with the Description of Two New Species.
International Journal of Primatology 29: 723–741.
The author of the last published systematic review of Cacajao recognized 2 subspecies of black-headed uakaris (black uakaris): Cacajao melanocephalus melanocephalus and C. m. ouakary. As a result of a series of black uakari surveys and collecting expeditions to several tributaries of the Rio Negro and of morphological and molecular analyses of museum specimens and specimens we collected during field expeditions, we reassess their taxonomy. We describe a newly discovered species of black uakari from the Rio Aracá, a left bank tributary of the Rio Negro, Amazonas, Brazil. We also show that ouakary is a junior synonym of melanocephalus and provide a new name and a new description for Cacajao melanocephalus melanocephalus in the Pico da Neblina region of Brazil and Venezuela. Based on genetic, morphological, and ecological evidence, we propose that there are 3 species of black uakaris. We named the Rio Aracá species Cacajao ayresi sp. nov. (Ayres uakari) in honor of the late José Márcio Ayres, a pioneer in uakari research and conservation. We named the Neblina black uakari Cacajao hosomi, after the Yanomami word for uakaris. The new taxonomic arrangement provided here implies that the conservation status of black uakaris needs to be reassessed.
Extra-Mediterranean glacial refuges in barred and common grass snakes (Natrix helvetica, N. natrix).
Scientific Reports 8, Article number: 1821 (2018). https://doi.org/10.1038/s41598-018-20218-2.
Extra-Mediterranean glacial refugia of thermophilic biota, in particular in northern latitudes, are controversial. In the present study we provide genetic evidence for extra-Mediterranean refugia in two species of grass snake. The refuge of a widely distributed western European lineage of the barred grass snake (Natrix helvetica) was most likely located in southern France, outside the classical refuges in the southern European peninsulas. One genetic lineage of the common grass snake (N. natrix), distributed in Scandinavia, Central Europe and the Balkan Peninsula, had two distinct glacial refuges. We show that one was located in the southern Balkan Peninsula. However, Central Europe and Scandinavia were not colonized from there, but from a second refuge in Central Europe. This refuge was located in between the northern ice sheet and the Alpine glaciers of the last glaciation and most likely in a permafrost region. Another co-distributed genetic lineage of N. natrix, now massively hybridizing with the aforementioned lineage, survived the last glaciation in a structured refuge in the southern Balkan Peninsula, according to the idea of ‘refugia-within-refugia’. It reached Central Europe only very recently. This study reports for the first time the glacial survival of a thermophilic egg-laying reptile species in Central Europe.
Phylogeographic Patterns in Africa and High Resolution Delineation of Genetic Clades in the Lion (Panthera leo).
Sci Rep 6, 30807 (2016). https://doi.org/10.1038/srep30807
Comparative phylogeography of African savannah mammals shows a congruent pattern in which populations in West/Central Africa are distinct from populations in East/Southern Africa. However, for the lion, all African populations are currently classified as a single subspecies (Panthera leo leo), while the only remaining population in Asia is considered to be distinct (Panthera leo persica). This distinction is disputed both by morphological and genetic data. In this study we introduce the lion as a model for African phylogeography. Analyses of mtDNA sequences reveal six supported clades and a strongly supported ancestral dichotomy with northern populations (West Africa, Central Africa, North Africa/Asia) on one branch and southern populations (North East Africa, East/Southern Africa and South West Africa) on the other. We review taxonomies and phylogenies of other large savannah mammals, illustrating that similar clades are found in other species. The described phylogeographic pattern is considered in relation to large scale environmental changes in Africa over the past 300,000 years, attributable to climate. Refugial areas, predicted by climate envelope models, further confirm the observed pattern. We support the revision of current lion taxonomy, as recognition of a northern and a southern subspecies is more parsimonious with the evolutionary history of the lion.
Gene flow between insular, coastal and interior populations of brown bears in Alaska.
Molecular Ecology 7(10): 1283-1292. https://doi.org/10.1046/j.1365-294x.1998.00440.x
The brown bears of coastal Alaska have been recently regarded as comprising from one to three distinct genetic groups. We sampled brown bears from each of the regions for which hypotheses of genetic uniqueness have been made, including the bears of the Kodiak Archipelago and the bears of Admiralty, Baranof and Chichagof (ABC) Islands in southeast Alaska. These samples were analysed with a suite of nuclear microsatellite markers. The ‘big brown bears’ of coastal Alaska were found to be part of the continuous continental distribution of brown bears, and not genetically isolated from the physically smaller ‘grizzly bears’ of the interior. By contrast, Kodiak brown bears appear to have experienced little or no genetic exchange with continental populations in recent generations. The bears of the ABC Islands, which have previously been shown to undergo little or no female‐mediated gene flow with mainland populations, were found not to be genetically isolated from mainland bears. The data from the four insular populations indicate that female and male dispersal can be reduced or eliminated by water barriers of 2–4 km and 7km in width, respectively.
Vocal Diversity and Taxonomy of Nomascus in Central Vietnam and Southern Laos.
International Journal of Primatology 31: 73–94.
Previous researchers suggested that gibbon song repertoire is genetically determined and song characteristics are useful for assessing systematic relationships. The southern white-cheeked crested gibbon is regarded as either a subspecies of Nomascus leucogenys or its own species (Nomascus siki). I studied vocal diversity among different wild populations of Nomascus in central Vietnam and southern Laos to assess their taxonomic relationships and to examine whether their vocal patterns correspond to forms previously described for Nomascus siki. I examined the songs of 7 Nomascus populations in Vietnam and Laos. I analyzed 192 song bouts from different gibbon groups including 173 phrases of 42 females and 192 phrases of 42 males. Linear discriminant analysis, classification trees, and multidimensional scaling revealed marked separation of groups in the northern and southern populations. Within the 2 geographic populations, there is little variability and the vocal characteristics exhibited no apparent cline. I conclude that the northern and southern geographic populations may represent 2 distinct taxa. I postulate that a taxonal boundary such as large rivers existing between southern Quang Binh province and northern Thua-Thien Hue province in Vietnam and northern Phou Xang He NBCA and southern Dong Phou Vieng NBCA in Laos has limited gene flow between the populations. Differing topographic features could also serve as a selective force for improved sound transmission in a highly territorial species, driving the divergence between the 2 populations.
Phylogenetic relationships of Mesoamerican spider monkeys (Ateles geoffroyi): Molecular evidence suggests the need for a revised taxonomy.
Molecular Phylogenetics and Evolution 82: 484-494.
Mesoamerican spider monkeys (Ateles geoffroyi sensu lato) are widely distributed from Mexico to northern Colombia. This group of primates includes many allopatric forms with morphologically distinct pelage color and patterning, but its taxonomy and phylogenetic history are poorly understood. We explored the genetic relationships among the different forms of Mesoamerican spider monkeys using mtDNA sequence data, and we offer a new hypothesis for the evolutionary history of the group. We collected up to ~800 bp of DNA sequence data from hypervariable region 1 (HV1) of the control region, or D-loop, of the mitochondrion for multiple putative subspecies of Ateles geoffroyi sensu lato. Both maximum likelihood and Bayesian reconstructions, using Ateles paniscus as an outgroup, showed that (1) A. fusciceps and A. geoffroyi form two different monophyletic groups and (2) currently recognized subspecies of A. geoffroyi are not monophyletic. Within A. geoffroyi, our phylogenetic analysis revealed little concordance between any of the classiﬁcations proposed for this taxon and their phylogenetic relationships, therefore a new classiﬁcation is needed for this group. Several possible clades with recent divergence times (1.7–0.8 Ma) were identiﬁed within Ateles geoffroyi sensu lato. Some previously recognized taxa were not separated by our data (e.g., A. g. vellerosus and A. g. yucatanensis), while one distinct clade had never been described as a different evolutionary unit based on pelage or geography (Ateles geoffroyi ssp. indet. from El Salvador). Based on well-supported phylogenetic relationships, our results challenge previous taxonomic arrangements for Mesoamerican spider monkeys. We suggest a revised arrangement based on our data and call for a thorough taxonomic revision of this group.
Integration of nuclear and mitochondrial gene sequences and morphology reveals unexpected diversity in the forest cobra (Naja melanoleuca) species complex in Central and West Africa (Serpentes: Elapidae)
Zootaxa 4455 (1): 068–098. http://www.mapress.com/j/zt/. ISSN1175-5334(online edition).
Cobras are among the most widely known venomous snakes, and yet their taxonomy remains incompletely understood, particularly in Africa. Here, we use a combination of mitochondrial and nuclear gene sequences and morphological data to diagnose species limits within the African forest cobra, Naja (Boulengerina) melanoleuca. Mitochondrial DNA sequences reveal deep divergences within this taxon. Congruent patterns of variation in mtDNA, nuclear genes and mor-phology support the recognition of five separate species, confirming the species status of N. subfulva and N. peroescobari, and revealing two previously unnamed West African species, which are described as new: Naja (Boulengerina) guineensis sp. nov. Broadley, Trape, Chirio, Ineich & Wüster, from the Upper Guinea forest of West Africa, and Naja (Boulengerina) savannula sp. nov. Broadley, Trape, Chirio & Wüster, a banded form from the savanna-forest mosaic of the Guinea and Sudanian savannas of West Africa. The discovery of cryptic diversity in this iconic group highlights our limited under-standing of tropical African biodiversity, hindering our ability to conserve it effectively.