Jennifer M. Lamb

Genetic monitoring detects an overlooked cryptic species and reveals the diversity and distribution of three invasive Rattus congeners in South Africa.

BackgroundSouth Africas long and extensive trade activity has ensured ample opportunities for exotic species introduction. Whereas the rich biodiversity of endemic southern African fauna has been the focus of many studies, invasive vertebrates are generally overlooked despite potential impacts on biodiversity, health and agriculture. Genetic monitoring of commensal rodents in South Africa which uncovered the presence of Rattus tanezumi, a South-East Asian endemic not previously known to occur in Africa, provided the impetus for expanded studies on all invasive Rattus species present.ResultsTo this end, intensified sampling at 28 South African localities and at one site in Swaziland, identified 149 Rattus specimens. Cytochrome b gene sequencing revealed the presence of two R. tanezumi, seven Rattus rattus and five Rattus norvegicus haplotypes in south Africa. Phylogenetic results were consistent with a single, recent R. tanezumi introduction and indicated that R. norvegicus and R. rattus probably became established following at least two and three independent introductions, respectively. Intra- and inter-specific diversity was highest in informal human settlements, with all three species occurring at a single metropolitan township site. Rattus norvegicus and R. rattus each occurred sympatrically with Rattus tanezumi at one and five sites, respectively. Karyotyping of selected R. rattus and R. tanezumi individuals identified diploid numbers consistent with those reported previously for these cryptic species. Ordination of bioclimatic variables and MaxEnt ecological niche modelling confirmed that the bioclimatic niche occupied by R. tanezumi in south Africa was distinct from that occupied in its naturalised range in south-east Asia suggesting that factors other than climate may influence the distribution of this species.ConclusionsThis study has highlighted the value of genetic typing for detecting cryptic invasive species, providing historical insights into introductions and for directing future sampling. The apparent ease with which a cryptic species can become established signals the need for broader implementation of genetic monitoring programmes. In addition to providing baseline data and potentially identifying high-risk introduction routes, the predictive power of ecological niche modelling is enhanced when species records are genetically verified.

Phylogeography and predicted distribution of African-Arabian and Malagasy populations of giant mastiff bats, Otomops spp. (Chiroptera: Molossidae)

ABSTRACT Otomops martiensseni is sparsely distributed throughout sub-Saharan Africa and southwestern Arabia (Yemen). Otomops madagascariensis from the dry portions of Madagascar is widely recognised to be a distinct species. Based on mitochondrial DNA sequences of the cytochrome b gene (1,004 base pairs; n = 50) and the control region (D-loop, 290 base pairs; n = 52), two Oriental outgroup species (O. wroughtoni and O. cf. formosus) formed a monophyletic clade that was the sister group to the Afro-Malagasy taxa, composed of O. martiensseni and O. madagascariensis. Within the Afro-Malagasy clade, we discovered three well-supported but genetically similar clades (inter-clade genetic distances of 3.4–4.4%) from 1) north-eastern Africa and Arabia, 2) African mainland except northeast Africa, and 3) Madagascar. Taken together, haplotype networks, estimated divergence times, regional species richness and historical demographic data tentatively suggested dispersal from Asia to Africa and Madagascar. To understand ecological determinants of phylogeographic, biogeographic and genetic structure, we assessed the potential distribution of O. martiensseni throughout sub-Saharan Africa with ecological niche modelling (MaxEnt) based on known point localities (n = 60). The species is predicted to occur mainly in woodlands and forests and in areas of rough topography. Continuity of suitable habitats supported our inferred high levels of continental gene flow (relatively low genetic distances), and suggested that factors other than habitat suitability have resulted in the observed phylogeographic structure (e.g., seasonal mass migrations of insects that might be tracked by these bats). Based on a Bayesian relaxed clock approach and two fossil calibration dates, we estimated that African and Oriental clades diverged at 4.2 Mya, Malagasy and African clades at 1.5 Mya, and African clades 1 and 2 at 1.2 Mya. Integrating phylogenetic, phylogeographic, population genetic and ecological approaches holds promise for a better understanding of biodiversity patterns and evolutionary processes.

Morphological and molecular assessment of the specific status of Mops midas (Chiroptera: Molossidae) from Madagascar and Africa

ABSTRACT The Molossidae bat Mops midas has a broad distribution across portions of Africa and is also known from Madagascar. The African populations have been referred to the subspecies M. m. midas and those from Madagascar to M. m. miarensis. The subspecific differences between these two forms have been called into question. However, largely due to the rarity of the Malagasy subspecies in collections, it has not been previously possible to address this point. Recent bat surveys on Madagascar have found that this species is relatively common in portions of the west and south; using these new collections, we address the question of the distinctiveness of miarensis. External measurements and soft-part anatomy, as well as cranial and dental measurements and structure, revealed few differences between the African and Malagasy populations. Further, molecular comparisons using 1080 bp of mitochondrial cytochrome b found a divergence of only 0.1% between South African and Malagasy populations, compared with a divergence of 13.3/13.5% between them and M. condylurus/M. leucostigma. Further, comparisons of 304 bp of the more variable mitochondrial d-loop revealed a divergence of only 1.2% between South African and Malagasy M. midas, compared with a divergence of 40.9/42.3% between them and M. condylurus/M. leucostigma. Consequently, we propose that no subspecific variation should be recognized in M. midas. A biogeographic analysis is presented with regards to movements of molossid bats between portions of eastern and southern Africa and Madagascar.

Toward a Molecular Phylogeny for the Molossidae (Chiroptera) of the Afro-Malagasy Region

We present phylogenetic information based on nuclear Rag2 and mitochondrial cytochrome b sequence data for six genera of Molossidae (Chaerephon, Mops, Mormopterus, Otomops, Sauromys, Tadarida) and 18 species, primarily from Africa and the Malagasy region (Madagascar and neighbouring islands), and further include sequences of 12 New World and African taxa sourced from GenBank. There is strong support for the monophyly of the Molossidae included in this study. The Malagasy region taxa Mormopterus jugularis and M. francoismoutoui are supported as a basal clade with an age of ≈ 31.2 MYR, and are not monophyletic with the South American M. kalinowskii. Asian Otomops wroughtoni and O. formosus and Afro-Malagasy O. martiensseni and O. madagascariensis form a strongly-supported ≈ 19.8 MYR-old clade, whose broader relationships among Molossidae are not clearly defined. There is strong support for a ≈ 17.2 MYR-old combined Chaerephon/Mops clade, in which members of these genera show some paraphyly. The monophyly of the genus Tadarida, represented in our analyses by T. brasiliensis from the New World and T. fulminons, T. aegyptiaca and T. teniotis from the Old World, is not upheld, although there is good support for a geographicallydisjunct ≈ 9.8 MYR-old grouping which includes C. jobimena (Madagascar), T. aegyptiaca (Africa) and T. brasiliensis (America). Sauromys is maintained as a monotypic genus, although there is moderate support for its association with T. fulminans and the Chaerephon/Mops clade, the latter of which comprises M. midas, M. leucostigma, M. condylurus, M. bakarii, C. pumilus, C. pusillus, C. leucogaster and C. atsinanana. An ≈ 8.4 MYR-old New World clade comprising representatives of Eumops, Nyctinomops and Molossus was well-supported.

Geographic and phylogeographic variation in Chaerephon leucogaster (Chiroptera: Molossidae) of Madagascar and the western Indian Ocean islands of Mayotte and Pemba

We examine patterns of morphological and genetic variation in Chaerephon leucogaster (family Molossidae) on Madagascar, Mayotte in the Comoros Archipelago, and the offshore Tanzanian island of Pemba. Five external, 10 cranial, and eight dental measurements of animals from different Malagasy populations (grouped according to bioclimatic regions) show differences in the degree of sexual dimorphism and size variation. Further, the population on Mayotte is largely identical in size to those from western Madagascar, and animals from Pemba are notably larger than those from Madagascar and Mayotte. Cytochrome b genetic distances across samples from these islands were low (maximum 0.0035) and animals from Pemba and Mayotte shared cytochrome b haplotypes with Malagasy bats. D-loop data showed some concordance between haplotype distribution, geographical position (latitude and island), and the bioclimatic zones. Animals from Pemba and Mayotte formed a unique D-loop haplotype, which was a minimum of six mutational steps different from Malagasy haplotypes. Within Madagascar, certain haplotypes were exclusive to the north (13°S latitude band) and arid southwest (22° and 23°S latitudes) regions. In general, there was no clear concordance between variation in haplotype distribution, latitude, altitude or gender. Where concordance occurred, the genetic distances involved were not sufficiently high to warrant the definition of new taxonomic units. Hence, based on current genetic information, patterns of morphological variation of the Madagascar populations and differences between Pemba and Mayotte/Madagascar are best explained as inter-population variation and may be adaptive, associated with different climatic regimes and associated ecological variables.

Cryptic lineages of little free-tailed bats, Chaerephon pumilus (Chiroptera: Molossidae) from southern Africa and the western Indian Ocean islands

We investigate mitochondrial DNA and craniometric variation in southern African and Malagasy populations of the small and morphologically variable, house-roosting molossid bat, Chaerephon pumilus in relation to Malagasy populations of the related, smaller-sized species, C. leucogaster. Both cytochrome b and D-loop sequences show C. leucogaster to be nested within C. pumilus sensu lato, with Malagasy C. pumilus forming a sister group to African C. pumilus and Malagasy C. leucogaster. Four distinct D-loop clades are found in southern African populations, all of which occur sympatrically in the greater Durban area of KwaZulu-Natal Province, whilst two of the Durban clades also characterize 1) northern KwaZulu-Natal and low-lying (<600 m) areas of Swaziland, and 2) ‘inland’ populations comprising the Kruger National Park and higher-lying (>600 m) areas of Swaziland. Clades from low-lying areas show evidence of historical demographic expansion around 3300–13 000 years ago (KwaZulu-Natal coastal clade, Clade A1) to 14 700–60 000 years ago (Durban clade, – Clade B1), whilst the inland clade (Clade B2a) was demographically more stable. The origin of these clades can be explained by sea level and vegetation changes hypothesized to follow the Last Glacial Maximum (LGM) after 18 000 years ago. Sympatric clades are shown to differ significantly in the proportional width of the braincase, and ongoing work will test evidence for acoustic and other morphological differences between them.

Experimental treatment-control studies of ecologically based rodent management in Africa: balancing conservation and pest management

Abstract Context. Rodent pests severely affect crop production, particularly in monocultures where one or two rodent pest species dominate. We predict higher species richness of native small mammal species in more heterogeneous mosaic (crop–fallow–bush) subsistence agro-ecosystems in Africa. Conservation and agro-ecological imperatives require that such diverse natural communities should be maintained and may benefit crop protection through limiting domination of pest species. Ecologically based rodent-management alternatives to rodenticides are urgently required and one such method (community trapping) is herein advocated. Aims. To provide baseline information on rodent and shrew communities in agro-ecosystems in three African countries and to demonstrate efficacy of ecologically based rodent management (EBRM) in Africa (e.g. community household trapping). Methods. Removal-trapping in a variety of agro-ecological habitats provided accurate small-mammal species lists. Intensive kill-trapping by rural agricultural communities was carried out experimentally where the efforts of communities were scientifically monitored by kill-trapping to measure impact on rodent numbers and the levels of post-harvest damage to stored grains. Key results. Our study revealed a high diversity of endemic species in agricultural habitats in Tanzania and Namibia (but not Swaziland) and the existence of undescribed and possibly rare species, some of which may be at risk of extinction from unchecked habitat transformation for agriculture. Treatment-control studies showed that communities in three African countries could effectively reduce pest rodent populations and rodent damage by intensive trapping on a daily basis in and around the community. Conclusions. Community trapping reduced pest rodent populations and damage to stored grains. Unlike the use of indiscriminate rodenticide, this practice is expected to have a negligible effect on beneficial non-target rodent and shrew species. Implications. Ecologically based rodent management approaches such as community trapping will conserve beneficial non-pest rodent communities and ultimately improve crop protection.

Morphological and genetic variation in Mormopterus jugularis (Chiroptera: Molossidae) in different bioclimatic regions of Madagascar with natural history notes

Abstract We investigated patterns of morphological and genetic variation in Mormopterus jugularis, an endemic Malagasy Molossidae. On the basis of external and cranio-dental measurements taken from adult specimens, the following conclusions can be drawn: there is notable sexual dimorphism, males being larger than females and there is no clear pattern of variation associated with bioclimatic, latitudinal or altitudinal zonation. DNA sequence analyses were based on 1078 nucleotides of the mt cytochrome b (cyt b) gene (n=20) and 351 nucleotides of the 5′ hypervariable region of the D-loop (n=50). A high haplotype diversity within M. jugularis (cyt b=0.995, D-loop=1.00) was combined with an absence of genetic structure. Analysis of molecular variance showed no significant grouping of haplotypes with latitude, longitude or altitude. D-loop diversity and neutrality analyses indicate that the Malagasy samples form a single population, which has been expanding for between 120,884 and 230,588 years. According to the MaxEnt potential distribution model, M. jugularis is predicted to occur ubiquitously across most of southern and central Madagascar, accounting for the observed genetic and morphological homogeneity of populations; observed specimen records north of 18°S occur in unsuitable habitats and may have arisen from recent expansion into synanthropic roosts. This species has a broad geographic distribution across much of Madagascar, encompassing the elevational range from 70 to 1750 m. The vast majority of known roosting sites are in human built structures, which are often shared with different species of Molossidae.

Cross-species chromosome painting in bats from Madagascar: the contribution of Myzopodidae to revealing ancestral syntenies in Chiroptera

The chiropteran fauna of Madagascar comprises eight of the 19 recognized families of bats, including the endemic Myzopodidae. While recent systematic studies of Malagasy bats have contributed to our understanding of the morphological and genetic diversity of the island’s fauna, little is known about their cytosystematics. Here we investigate karyotypic relationships among four species, representing four families of Chiroptera endemic to the Malagasy region using cross-species chromosome painting with painting probes of Myotis myotis: Myzopodidae (Myzopoda aurita, 2n = 26), Molossidae (Mormopterus jugularis, 2n = 48), Miniopteridae (Miniopterus griveaudi, 2n = 46), and Vespertilionidae (Myotis goudoti, 2n = 44). This study represents the first time a member of the family Myzopodidae has been investigated using chromosome painting. Painting probes of M. myotis were used to delimit 29, 24, 23, and 22 homologous chromosomal segments in the genomes of M. aurita, M. jugularis, M. griveaudi, and M. goudoti, respectively. Comparison of GTG-banded homologous chromosomes/chromosomal segments among the four species revealed the genome of M. aurita has been structured through 14 fusions of chromosomes and chromosomal segments of M. myotis chromosomes leading to a karyotype consisting solely of bi-armed chromosomes. In addition, chromosome painting revealed a novel X-autosome translocation in M. aurita. Comparison of our results with published chromosome maps provided further evidence for karyotypic conservatism within the genera Mormopterus, Miniopterus, and Myotis. Mapping of chromosomal rearrangements onto a molecular consensus phylogeny revealed ancestral syntenies shared between Myzopoda and other bat species of the infraorders Pteropodiformes and Vespertilioniformes. Our study provides further evidence for the involvement of Robertsonian (Rb) translocations and fusions/fissions in chromosomal evolution within Chiroptera.

DNA sequence analyses reveal co-occurrence of novel haplotypes of Fasciola gigantica with F. hepatica in South Africa and Zimbabwe

The aim of this study was to identify and determine the genetic diversity of Fasciola species in cattle from Zimbabwe, the KwaZulu-Natal and Mpumalanga provinces of South Africa and selected wildlife hosts from Zimbabwe. This was based on analysis of DNA sequences of the nuclear ribosomal internal transcribed spacer (ITS1 and 2) and mitochondrial cytochrome oxidase 1 (CO1) regions. The sample of 120 flukes was collected from livers of 57 cattle at 4 abattoirs in Zimbabwe and 47 cattle at 6 abattoirs in South Africa; it also included three alcohol-preserved duiker, antelope and eland samples from Zimbabwe. Aligned sequences (ITS 506 base pairs and CO1 381 base pairs) were analyzed by neighbour-joining, maximum parsimony and Bayesian inference methods. Phylogenetic trees revealed the presence of Fasciola gigantica in cattle from Zimbabwe and F. gigantica and Fasciola hepatica in the samples from South Africa. F. hepatica was more prevalent (64%) in South Africa than F. gigantica. In Zimbabwe, F. gigantica was present in 99% of the samples; F. hepatica was found in only one cattle sample, an antelope (Hippotragus niger) and a duiker (Sylvicapra grimmia). This is the first molecular confirmation of the identity Fasciola species in Zimbabwe and South Africa. Knowledge on the identity and distribution of these liver flukes at molecular level will allow disease surveillance and control in the studied areas.