Pattern of shape variation in the eastern African gerbils of the genus Gerbilliscus (Rodentia,Muridae): Environmental correlations and implication for taxonomy and systematics

Gerbilliscus has been in recent years the subject of new molecular and karyological investigations that shed new light on the evolutionary processes of this taxon. However, the patterns of phenotypic diversification of Gerbilliscus remain poorly understood. Furthermore, the molecular phylogenetic analyses posed new questions concerning the systematics and taxonomy of the whole genus and revealed the possible occurrence of cryptic species and hence the need to carry out a taxonomic revision.We used geometric morphometrics to investigate the adaptive value of morphological changes and to elucidate the systematic relationships and taxonomic status of the Gerbilliscus species of east Africa.Our results show concordance between morphological and genetic species boundaries. However, the observed morphological differences appear not only related to hereditary characters. In fact, the correlation with the climatic variables suggests an adaptive value of shape changes related to different trophic resources availability.Finally, discriminant analysis of the eastern Africa Gerbilliscus species highlight the distinctiveness of G. vicinus, clearly separated from G. robustus and G. nigricaudus.     

Systematics and evolution of the subfamily Gerbillinae (Mammalia, Rodentia, Muridae)

Although they represent a quarter of the mammalian species, the evolutionary relationships among as well as within, the main murid lineages are still controversial. The subfamily Gerbillinae is no exception as previous studies based on morphological, karyotypical, and allozyme characters are highly incongruent. Here, we present the first molecular phylogeny for gerbils based on cytochrome b and 12S rRNA mitochondrial genes. Results are largely congruent between the two genes as well as with the concatenated data set with most of the nodes being well-supported. Based on the topologies retrieved here, we (1) propose the identification of three main clades, (2) support the split of Tatera genus into an Asian and an African group, the latter including Gerbillurus species, and (3) provide some evidence towards the inaccuracy of subgeneric divisions within both Gerbillus and Meriones. In addition, the sharp contrast between the genetic characters and morphological data sets suggest high levels of convergence, probably as a result of strong environmental constraints imposed on these rodents adapted to arid and semi-arid regions. Finally, molecular datings for the various cladogenetic events are in good agreement with the known gerbilline fossil record and support an African origin with subsequent migrations to Asia.     

Mitochondrial phylogeny reveals differential modes of chromosomal evolution in the genus Tatera (Rodentia: Gerbillinae) in Africa

The African gerbils of the genus Tatera are widespread and abundant throughout sub-Saharan Africa. There is still today a certain controversy concerning the taxonomy of these rodents and very few attempts have been made to assess their systematic relationships. The present paper introduces findings based on the partial sequences of cytochrome b (495 bp) and the 16S rRNA (469 bp) mitochondrial genes of six (T. robusta, T. nigricauda, T. vicina, T. leucogaster, T. valida, and T. kempi) species together with two additional taxa. We also report the karyotypes of T. vicina and T. leucogaster. We propose that T. vicina should be considered as a valid species and show the monophyly of the robusta species group, with the exclusion of T. leucogaster. Our results show there is a different chromosomal evolutionary pattern within the two major lineages, which is recognizable through molecular phylogenetics. One is characterized by karyotype stability and the other by a considerable number of chromosomal rearrangements. The lineage divergence coincides with the formation of the East African Rift. The processes that led to the origin of the East African species seem to be related to the subsequent climatic changes, which caused cyclic contraction and expansion of the savannah biomes. Furthermore, geological activities that characterized East Africa during Plio-Pleistocene may also have contributed to lineage divergence.     

Species delimitation in the Acomys cahirinus–dimidiatus complex (Rodentia, Muridae) inferred from chromosomal and morphological analyses

Our earlier chromosome banding studies of Acomys cahirinus and Acomys dimidiatus (the latter long considered to be a subspecies of the former) revealed that, despite very close diploid numbers (36 vs. 38), these taxa possess sharply different karyotypes and undoubtedly belong to different species. In this context, the taxonomic status and the relationship between the two chromosomal forms in Sinai (2 n  = 36) and Israel (2 n  = 38), chromosomally homozygous across a vast range except for a very narrow hybrid zone, remain poorly documented. Neither of these forms have previously been studied by chromosome banding; thus, the exact nature of chromosomal differences as well as the species to which these forms should be assigned remain unknown. Here, we present the data on comparative G-banding analysis and morphometrics of Acomys from Israel, Sinai, and Saudi Arabia, and a hybrid obtained in laboratory crosses between latter two. The analysis revealed that karyotype of Acomys from Israel is identical to that of Acomys from Saudi Arabia and both are different from that of Acomys from Sinai by one Robertsonian fusion. Therefore, karyotypically, all three are very different from A. cahirinus . It follows from the study that Sinai and probably Arabian peninsula and Minor Asia must be excluded from geographical distribution of A. cahirinus , which is limited from West Sahara to Egypt along Nile river (except Sinai). Furthermore, the synthesis of chromosomal and recent molecular data suggests a phylogeographical scenario explaining the modern distribution of Acomys in the Sinai and Arabian peninsulas and permits the update of the taxonomic status of these populations.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 203–214.     

Taxonomic hypotheses regarding the genus Gerbillus (Rodentia,Muridae, Gerbillinae) based on molecular analyses of museum specimens

Methodological improvements now allow routine analyses of highly degraded DNA samples as found in museum specimens. Using these methods could be useful in studying such groups as rodents of the genus Gerbillus for which i) the taxonomy is still highly debated, ii) collection of fresh specimens may prove difficult. Here we address precise taxonomic questions using a small portion of the cytochrome b gene obtained from 45 dry skin/skull museum samples (from 1913 to 1974) originating from two African and three Asian countries. The specimens were labelled Gerbillus gerbillus, Gerbillus andersoni, Gerbillus nanus, Gerbillus amoenus, Gerbillus perpallidus and Gerbillus pyramidum, and molecular results mostly confirmed these assignations. The close relationship between Gerbillus nanus (Asian origin) and Gerbillus amoenus (African origin) confirmed that they represent vicariant sibling species which differentiated in allopatry on either side of the Red Sea. In the closely related Gerbillus perpallidus and Gerbillus pyramidum, specimens considered as belonging to one Gerbillus pyramidum subspecies (Gerbillus pyramidum floweri) appeared closer to Gerbillus perpallidus suggesting that they (Gerbillus pyramidum floweri and Gerbillus perpallidus) may represent a unique species, distributed on both sides of the Nile River, for which the correct name should be Gerbillus floweri. Furthermore, the three other Gerbillus pyramidum subspecies grouped together with no apparent genetic structure suggesting that they may not yet represent genetically differentiated lineages. This study confirms the importance of using these methods on museum samples, which can open new perspectives in this particular group as well as in other groups of interest.     

Systematics of the dung beetle tribe Sisyphini Mulsant (Scarabaeidae: Scarabaeinae) inferred from a molecular phylogeny and biogeography of southern African species

The tribe Sisyphini Mulsant was recently redefined following the transfer of the endemic southern African genus Epirinus Dejean from the polyphyletic tribe Deltochilini Lacordaire. A molecular phylogeny of the southern African members of Sisyphini supports Epirinus as sister to Sisyphus Latreille and recovered three major clades in Sisyphus classified here as subgenera Sisyphus (Neosisyphus Müller) stat. rev. , Sisyphus (Parasisyphus Barbero, Palestrini & Zunino) stat.n. and Sisyphus (Sisyphus) stat.n. A molecular clock analysis suggests that Sisyphus and Epirinus diverged from their last common ancestor during the Lower to Middle Oligocene (c. 29.37 Ma). Biogeographical analysis indicated that southern African Sisyphus species are centred in the east and northeast in Highveld grassland and warmer savannah regions. By contrast, Epirinus species are largely restricted to the southwest and southeast in the cooler winter and bimodal rainfall regions plus arid highland Karoo and Highveld grasslands. Based on morphological and biogeographical differences between Epirinus and Sisyphus, we propose that the monogeneric Epirinus be placed in its own tribe, Epirinini van Lansberge stat. rev.     

Mitochondrial phylogeny of African wood mice, genus Hylomyscus (Rodentia, Muridae): implications for their taxonomy and biogeography

This paper investigates the usefulness of two mitochondrial genes (16S rRNA and cytochrome b) to solve taxonomical difficulties within the genus Hylomyscus and to infer its evolutionary history. Both genes proved to be suitable molecular markers for diagnosis of Hylomyscus species. Nevertheless the resolving powers of these two genes differ, and with both markers (either analyzed singly or in combination), some nodes remain unresolved. This is probably related to the fact that the species emerged during a rapid diversification event that occurred 2-6 Myr ago (4-5 Myr ago for most divergence events). Our molecular data support the recognition of an "aeta" group, while the "alleni" and "parvus" groups are not fully supported. Based on tree topology and genetic divergence, two taxa generally recognized as subspecies should be elevated at the species level (H. simus and H. cf kaimosae). H. stella populations exhibit ancient haplotype segregation that may represent currently unrecognized allopatric species. The existence of cryptic species within H. parvus is questioned. Finally, three potentially new species may occur in West Central Africa. The Congo and Oubangui Rivers, as well as the Volta and Niger Rivers and/or the Dahomey gap could have formed effective barriers to Hylomyscus species dispersal, favoring their speciation in allopatry. The pronounced shifts in African climate during the late Pliocene and Miocene, which resulted in major changes in the distribution and composition of the vegetation, could have promoted speciation within the genus (refuge theory). Future reports should focus on the geographic distribution of Hylomyscus species in order to get a better understanding of the evolutionary history of the genus.     

Molecular phylogeny and biogeography of Oriental voles: genus Eothenomys (Muridae, Mammalia)

Oriental voles of the genus Eothenomys are predominantly distributed along the Southeastern shoulder of the Qinghai-Tibetan Plateau. Based on phylogenetic analyses of the mitochondrial cytochrome b gene (1143 bp) obtained from 23 specimens (eight species) of Oriental voles collected from this area, together with nucleotide sequences from six specimens (two species) of Japanese red-backed voles (Eothenomys andersoni and Eothenomys smithii) and five species of the closely related genus Clethrionomys, we revised the systematic status of Eothenomys. We also tested if vicariance could explain the observed high species diversity in this area by correlating estimated divergence times to species distribution patterns and corresponding paleo-geographic events. Our results suggest that: (1) the eight species of Oriental voles form a monophyletic group with two distinct clades, and that these two clades should be considered as valid subgenera--Eothenomys and Anteliomys; (2) Eothenomys eleusis and Eothenomys miletus are not independent species; (3) Japanese red-backed voles are more closely related to the genus Clethrionomys than to continental Asian Eothenomys taxa; and (4) the genus Clethrionomys, as presently defined, is paraphyletic. In addition, the process of speciation of Oriental voles appears to be related to the Trans-Himalayan formation via three recent uplift events of the Qinghai-Tibetan Plateau within the last 3.6 million years, as well as to the effects of the mid-Quaternary ice age.     

Evolutionary systematics in African gerbilline rodents of the genus Gerbilliscus: inference from mitochondrial genes

Gerbilliscus has recently been proposed as an endemic African rodent genus distinct from the Asian Tatera. A molecular phylogeny of the genus, including nine species from southern, western and eastern Africa, is presented here based on the analysis of the cytochrome b and 16S mitochondrial genes. With an adequate taxonomic sampling over a wide geographic range, we here provide a clear picture of the phylogenetic relationships between species and species groups in this genus. Three distinct clades were resolved, corresponding to major geographical subdivisions: an eastern clade that possibly diverged first, then a southern and a western clades which appeared later. We suggest two possible hypotheses concerning the dispersal of the genus across Africa, considering also the patterns of karyotypic variation. Finally, we discuss the taxonomic status of G. gambianus and the relationships between Gerbillurus and Gerbilliscus, as previous studies have suggested that the former should be included in the latter. Our data seem to support the synonymy of the two taxa and suggest that Gerbillurus and Gerbilliscus lineages diverged from a common ancestor appeared in eastern Africa.     

Systematics of the genus Capra inferred from mitochondrial DNA sequence data

Traditional classification in the genus Capra is based mainly on horn morphology. However, previous investigations based on allozyme data are not consistent with this classification. We thus reexamined the evolutionary history of the genus by analyzing mitochondrial DNA (mtDNA) sequence variation. We collected bone samples from museums or dead animals found in the field. Thirty-four individuals were successfully sequenced for a portion of the mtDNA cytochrome b gene and control region (500 bp in total). We obtained a star-like phylogeny supporting a rapid radiation of the genus. In accordance with traditional classification, mtDNA data support the presence of two clades in the Caucasus and the hypothesis of a domestication event in the Fertile Crescent. However, in conflict with morphology, we found that C. aegagrus and C. ibex are polyphyletic species, and we propose a new scenario for Capra immigration into Europe.     

A genome-wide phylogeny and the diversification of genus Liriomyza (Diptera: Agromyzidae) inferred from anchored phylogenomics

The genus Liriomyza Mik (Diptera: Agromyzidae) is a diverse and globally distributed group of acalyptrate flies. Phylogenetic relationships among Liriomyza species have remained incompletely investigated and have never been fully addressed using molecular data. Here, we reconstruct the phylogeny of the genus Liriomyza using various phylogenetic methods (maximum likelihood, Bayesian inference, and gene tree coalescence) on target-capture-based phylogenomic datasets (nucleotides and amino acids) obtained from anchored hybrid enrichment (AHE). We have recovered tree topologies that are nearly congruent across all data types and methods, and individual clade support is strong across all phylogenetic analyses. Moreover, defined morphological species groups and clades are well-supported in our best estimates of the molecular phylogeny. Liriomyza violivora (Spencer) is a sister group to all remaining sampled Liriomyza species, and the well-known polyphagous vegetable pests [L. huidobrensis (Blanchard), L. langei Frick, L. bryoniae. (Kaltenbach), L. trifolii (Burgess), L. sativae Blanchard, and L. brassicae (Riley)]. belong to multiple clades that are not particularly closely related on the trees. Often, closely related Liriomyza species feed on distantly related host plants. We reject the hypothesis that cophylogenetic processes between Liriomyza species and their host plants drive diversification in this genus. Instead, Liriomyza exhibits a widespread pattern of major host shifts across plant taxa. Our new phylogenetic estimate for Liriomyza species provides considerable new information on the evolution of host-use patterns in this genus. In addition, it provides a framework for further study of the morphology, ecology, and diversification of these important flies.     

Molecular phylogeny of Turkish Trachurus species (Perciformes: Carangidae) inferred from mitochondrial DNA analyses

Genetic variation among three species of Trachurus (T. trachurus, T. mediterraneus and T. picturatus) from Turkey was investigated by phylogenetic analysis of the entire mtDNA control region (CR) (862 bp, n = 182) and partial cytochrome (cyt) b (239 bp, n = 174) sequences. Individuals were collected at nine stations in four geographic locations: North‐eastern Mediterranean Sea, Aegean Sea, Sea of Marmara and Black Sea. Polymerase chain reaction‐direct sequencing of the CR and the partial cyt b genes produced 28 and 131 distinct haplotypes, respectively. Maximum likelihood, neighbour‐joining and maximum parsimony methods produced similar tree topologies. The results of both CR and cyt b sequence analyses revealed the existence of several species‐specific nucleotide sites that can be used to discriminate between the three species. Genetic distances indicated that T. mediterraneus and T. picturatus are more closely related to each other than either is to T. trachurus. Inter‐nucleotide and intra‐nucleotide diversities of T. picturatus were larger than those of T. mediterraneus and T. trachurus. There was no evidence of a geographical difference in haplotype frequencies of these two mtDNA regions to be clustered.     

Phylogenetic relationships in genus Niviventer (Rodentia: Muridae) in China inferred from complete mitochondrial cytochrome b gene

Chinese species of the genus Niviventer, predominantly distributed in the southeastern Tibetan Plateau and in Taiwan, are a diverse group and have not yet received a thorough molecular phylogenetic analysis. Here, we reconstructed the phylogenetic relationships of 32 specimens representing nine Chinese species of Niviventer, based on sequences of the complete mitochondrial cytochrome b gene. Maximum parsimony, maximum likelihood and Bayesian analysis resulted in three consistent trees, each supported by high bootstrap values. The results showed that the Niviventer species included here are monophyletic. The nine species were classified into three distinct clades: clade A with Niviventer brahma, N. confucianus, N. coxingi, N. culturatus, N. eha and N. fulvescens; clade B with N. andersoni and N. excelsior; clade C with N. cremoriventer. Our results also suggested that N. culturatus should be a valid species rather than a subspecies of N. confucianus. Divergence times among species were calibrated according to the middle-late Pleistocene (1.2-0.13 Mya) fossil records of N. confucianus. The results demonstrated that the first radiation event of the genus Niviventer occurred in early Pleistocene (about 1.66 Mya), followed by the divergence of clades A and B at about 1.46 Mya. Most of the extant Niviventer species appeared during early to middle Pleistocene (about 1.29-0.67 Mya). These divergence times are coincidental with the last uplift events of the Tibetan Plateau, Kun-Huang movement, Pleistocene glaciations and the vicariant formation of Taiwan Strait. Consequently geographical events and Pleistocene glaciations have played a great role in the diversification of Niviventer.     

Molecular phylogenetic analyses indicate paraphyly of the genus Hybomys (Rodentia: Muridae): Taxonomic implications

Widely distributed in Guineo‐Congolian forests, the genus Hybomys is represented by two species complexes (univittatus and trivirgatus), each restricted to one distinct forest block. In the last revision, these two species complexes were considered as distinct subgenera (Hybomys and Typomys). Previous morphological and karyological studies identified an important divergence between these two subgenera and raised the question of their taxonomic status (subgenus or genus). The number of species within this genus is also a matter of discussion: nine forms were described but only six (H. badius, H. basilii, H. lunaris, H. planifrons, H. trivirgatus, and H. univitttatus) are currently recognized as distinct species, the three others (H. pearcei, H. eisentrauti, and H. rufocanus) being considered as synonyms. The monophyly of the genus and its species have never been previously investigated with DNA sequence data. In this study, we combined mitochondrial and nuclear data (for a total of 3,264 nucleotide characters) to test the monophyly of Hybomys and to assess the specific status of H. eisentrauti and H. rufocanus. Our results highlight the paraphyly of the genus: members of the H. univittatus species complex appeared closely related to the genera Stochomys and Dephomys; representatives of H. trivirgatus are the sister clade of the node grouping Stochomys, Dephomys and member of the H. univittatus species complex. Combined with previous morphological findings, our results suggest that Typomys and Hybomys should be considered as two distinct genera. Based on tree topology and genetic distances, we propose to consider H. rufocanus as a valid species, distinct from H. univittaus, and to consider H. badius and H. eisentrauti as junior synonyms of H. rufocanus.     

Systematics and diversification of Praomys species (Rodentia: Muridae) endemic to the Cameroon Volcanic Line (West Central Africa)

Missoup, A.D., Nicolas, V., Wendelen, W., Keming, E., Bilong Bilong, C.F., Couloux, A., Atanga, E., Hutterer, R. & Denys, C. (2012). Systematics and diversification of Praomys species (Rodentia: Muridae) endemic to the Cameroon Volcanic Line (West Central Africa). —Zoologica Scripta, 41, 327–345. Our integrative approach combines two mitochondrial genes (16S and cyt b gene), two nuclear genes (exon 10 GHR and exon 1 IRBP) and craniometrical data to test the status and to infer phylogenetic relationships of the three Praomys Cameroon Volcanic Line endemics (P. hartwigi, P. morio and P. obscurus). The taxonomic rank of the principal genus group is assessed and the mode of diversification of species of the P. tullbergi complex in Afrotropical forests is discussed based on estimates of times to the most recent common ancestors and on tree topologies. This study documents for the first time the molecular and morphometrical distinctiveness of P. hartwigi and P. morio within the P. tullbergi species complex. Further studies including specimens of P. hartwigi from all its distribution range are needed to conclude on the status of P. obscurus. The monophyly of the genus Praomys is refuted. Times to the most recent common ancestors of major clades within the P. tullbergi species complex are estimated for the last 2.5 Mya and during the last 1 or 2 Mya for different species or forms. The lowland forest refuge hypothesis might well explain the diversification of P. misonnei, P. rostratus and P. tullbergi in the guineo‐congolese forest block. The isolation of montane forests could have facilitated the divergence between the two montane forest forms P. hartwigi and P. obscurus and between populations of P. morio from the continent and those from the island of Bioko. Praomys populations (species) that inhabit the Cameroon Volcanic Line Praomys probably originated as lowland forms subsequently specialized to highland conditions.     

Biogeography and molecular phylogeny of the genus Schizothorax (Teleostei: Cyprinidae) in China inferred from cytochrome b sequences

Aim To test a vicariant speciation hypothesis derived from geological evidence of large‐scale changes in drainage patterns in the late Miocene that affected the drainages in the south‐eastern Tibetan Plateau. Location The Tibetan Plateau and adjacent areas. Methods The cytochrome b DNA sequences of 30 species of the genus Schizothorax from nine different river systems were analysed. These DNA sequences were analysed using parsimony, maximum likelihood and Bayesian methods. The approximately unbiased and Shimodaira–Hasegawa tests were applied to evaluate the statistical significance of the shortest trees relative to alternative hypotheses. Dates of divergences between lineages were estimated using the nonparametric rate smoothing method, and confidence intervals of dates were obtained by parametric bootstrapping. Results The phylogenetic relationships recovered from molecular data were inconsistent with traditional taxonomy, but apparently reflected geographical associations with rivers. Within the genus Schizothorax, we observed a divergence between the lineages from the Irrawaddy–Lhuit and Tsangpo–Parlung rivers, and tentatively dated this vicariant event back to the late Miocene (7.3–6.8 Ma). We also observed approximately simultaneous geographical splits within drainages of the south‐eastern Tibetan Plateau, the Irrawaddy, the Yangtze and the Mekong–Salween rivers in the late Miocene (7.1–6.2 Ma). Main conclusions Our molecular evidence tentatively highlights the importance of palaeoriver connections and the uplift of the Tibetan Plateau in understanding the evolution of the genus Schizothorax. Molecular estimates of divergence times allowed us to date these vicariant scenarios back to the late Miocene, which agrees with geological suggestions for the separation of these drainages caused by tectonic uplift in south‐eastern Tibet. Our results indicated the substantial role of vicariant‐based speciation in shaping the current distribution pattern of the genus Schizothorax.     

A phylogeny of Chinese species in the genus Phrynocephalus (Agamidae) inferred from mitochondrial DNA sequences

We investigated the phylogenetic relationships among most Chinese species of lizards in the genus Phrynocephalus (118 individuals collected from 56 populations of 14 well-defined species and several unidentified specimens) using four mitochondrial gene fragments (12S rRNA, 16S rRNA, cytochrome b, and ND4-tRNA(LEU)). The partition-homogeneity tests indicated that the combined dataset was homogeneous, and maximum-parsimony (MP), neighbor-joining (NJ), maximum-likelihood (ML) and Bayesian (BI) analyses were performed on this combined dataset (49 haplotypes including outgroups for 2058bp in total). The maximum-parsimony analysis resulted in 24 equally parsimonious trees, and their strict consensus tree shows that there are two major clades representing the Chinese Phrynocephalus species: the viviparous group (Clade A) and the oviparous group (Clade B). The trees derived from Bayesian, ML, and NJ analyses were topologically identical to the MP analysis except for the position of P. mystaceus. All analyses left the nodes for the oviparous group, the most basal clade within the oviparous group, and P. mystaceus unresolved. The phylogenies further suggest that the monophyly of the viviparous species may have resulted from vicariance, while recent dispersal may have been important in generating the pattern of variation among the oviparous species.