Steven M. Goodman

Retroviral envelope syncytin capture in an ancestrally diverged mammalian clade for placentation in the primitive Afrotherian tenrecs

Significance Syncytins are genes of retroviral origin that have been captured by their host as symbionts for a function in placentation. They can mediate cell–cell fusion, consistent with their ancestral retroviral envelope gene status, and are involved in fusion of mononucleate trophoblast cells to form the syncytial layer—the syncytiotrophoblast—of the feto–maternal interface. We proposed that such genes have been pivotal for the emergence of placental mammals from egg-laying animals and should be present all along the Placentalia radiation. We searched for syncytins in a superorder of eutherian mammals that emerged ancestrally during the Cretaceous terrestrial revolution and identified syncytin-Ten1, conserved over millions years of evolution of the Afrotherian tenrecs, regarded as among the most primitive of living mammals. Syncytins are fusogenic envelope (env) genes of retroviral origin that have been captured for a function in placentation. Syncytins have been identified in Euarchontoglires (primates, rodents, Leporidae) and Laurasiatheria (Carnivora, ruminants) placental mammals. Here, we searched for similar genes in species that retained characteristic features of primitive mammals, namely the Malagasy and mainland African Tenrecidae. They belong to the superorder Afrotheria, an early lineage that diverged from Euarchotonglires and Laurasiatheria 100 Mya, during the Cretaceous terrestrial revolution. An in silico search for env genes with full coding capacity within a Tenrecidae genome identified several candidates, with one displaying placenta-specific expression as revealed by RT-PCR analysis of a large panel of Setifer setosus tissues. Cloning of this endogenous retroviral env gene demonstrated fusogenicity in an ex vivo cell–cell fusion assay on a panel of mammalian cells. Refined analysis of placental architecture and ultrastructure combined with in situ hybridization demonstrated specific expression of the gene in multinucleate cellular masses and layers at the materno–fetal interface, consistent with a role in syncytium formation. This gene, which we named “syncytin-Ten1,” is conserved among Tenrecidae, with evidence of purifying selection and conservation of fusogenic activity. To our knowledge, it is the first syncytin identified to date within the ancestrally diverged Afrotheria superorder.

Working at the interface of phylogenetics and population genetics: a biogeographical analysis of Triaenops spp. (Chiroptera: Hipposideridae)

New applications of genetic data to questions of historical biogeography have revolutionized our understanding of how organisms have come to occupy their present distributions. Phylogenetic methods in combination with divergence time estimation can reveal biogeographical centres of origin, differentiate between hypotheses of vicariance and dispersal, and reveal the directionality of dispersal events. Despite their power, however, phylogenetic methods can sometimes yield patterns that are compatible with multiple, equally well‐supported biogeographical hypotheses. In such cases, additional approaches must be integrated to differentiate among conflicting dispersal hypotheses. Here, we use a synthetic approach that draws upon the analytical strengths of coalescent and population genetic methods to augment phylogenetic analyses in order to assess the biogeographical history of Madagascars Triaenops bats (Chiroptera: Hipposideridae). Phylogenetic analyses of mitochondrial DNA sequence data for Malagasy and east African Triaenops reveal a pattern that equally supports two competing hypotheses. While the phylogeny cannot determine whether Africa or Madagascar was the centre of origin for the species investigated, it serves as the essential backbone for the application of coalescent and population genetic methods. From the application of these methods, we conclude that a hypothesis of two independent but unidirectional dispersal events from Africa to Madagascar is best supported by the data.

Geogenetic patterns in mouse lemurs (genus Microcebus) reveal the ghosts of Madagascar's forests past

Phylogeographic analysis can be described as the study of the geological and climatological processes that have produced contemporary geographic distributions of populations and species. Here, we attempt to understand how the dynamic process of landscape change on Madagascar has shaped the distribution of a targeted clade of mouse lemurs (genus Microcebus) and, conversely, how phylogenetic and population genetic patterns in these small primates can reciprocally advance our understanding of Madagascars prehuman environment. The degree to which human activity has impacted the natural plant communities of Madagascar is of critical and enduring interest. Today, the eastern rainforests are separated from the dry deciduous forests of the west by a large expanse of presumed anthropogenic grassland savanna, dominated by the Family Poaceae, that blankets most of the Central Highlands. Although there is firm consensus that anthropogenic activities have transformed the original vegetation through agricultural and pastoral practices, the degree to which closed-canopy forest extended from the east to the west remains debated. Phylogenetic and population genetic patterns in a five-species clade of mouse lemurs suggest that longitudinal dispersal across the island was readily achieved throughout the Pleistocene, apparently ending at ∼55 ka. By examining patterns of both inter- and intraspecific genetic diversity in mouse lemur species found in the eastern, western, and Central Highland zones, we conclude that the natural environment of the Central Highlands would have been mosaic, consisting of a matrix of wooded savanna that formed a transitional zone between the extremes of humid eastern and dry western forest types.

Highly diverse morbillivirus-related paramyxoviruses in wild fauna of the southwestern Indian Ocean Islands: evidence of exchange between introduced and endemic small mammals.

ABSTRACT The Paramyxoviridae form an increasingly diverse viral family, infecting a wide variety of different hosts. In recent years, they have been linked to disease emergence in many different animal populations and in humans. Bats and rodents have been identified as major animal populations capable of harboring paramyxoviruses, and host shifting between these animals is likely to be an important driving factor in the underlying evolutionary processes that eventually lead to disease emergence. Here, we have studied paramyxovirus circulation within populations of endemic and introduced wild small mammals of the southwestern Indian Ocean region and belonging to four taxonomic orders: Rodentia, Afrosoricida, Soricomorpha, and Chiroptera. We report elevated infection levels as well as widespread paramyxovirus dispersal and frequent host exchange of a newly emerging genus of the Paramyxoviridae, currently referred to as the unclassified morbillivirus-related viruses (UMRVs). In contrast to other genera of the Paramyxoviridae, where bats have been shown to be a key host species, we show that rodents (and, in particular, Rattus rattus) are significant spreaders of UMRVs. We predict that the ecological particularities of the southwestern Indian Ocean, where small mammal species often live in densely packed, multispecies communities, in combination with the increasing invasion of R. rattus and perturbations of endemic animal communities by active anthropological development, will have a major influence on the dynamics of UMRV infection. IMPORTANCE Identification of the infectious agents that circulate within wild animal reservoirs is essential for several reasons: (i) infectious disease outbreaks often originate from wild fauna; (ii) anthropological expansion increases the risk of contact between human and animal populations and, as a result, the risk of disease emergence; (iii) evaluation of pathogen reservoirs helps in elaborating preventive measures to limit the risk of disease emergence. Many paramyxoviruses for which bats and rodents serve as major reservoirs have demonstrated their potential to cause disease in humans and animals. In the context of the biodiversity hot spot of southwestern Indian Ocean islands and their rich endemic fauna, we show that highly diverse UMRVs exchange between various endemic animal species, and their dissemination likely is facilitated by the introduced Rattus rattus. Hence, many members of the Paramyxoviridae appear well adapted for the study of the viral phylodynamics that may be associated with disease emergence.

A new species of Macrotarsomys (Rodentia: Muridae: Nesomyinae) from southwestern Madagascar

ABSTRACT A new species of Macrotarsomys, M. petteri (Rodentia: Muridae: Nesomyinae), is described based on a single specimen taken during a 2003 biological survey of the Forêt des Mikea in southwestern Madagascar. This is the third species known in this endemic genus, and all are confined to the dry forest formations of western Madagascar. The region where M. petteri occurs is a unique transitional forest habitat that is under considerable threat from human-induced habitat degradation and steps need to be swiftly taken to protect the Forêt des Mikea.

A new species of rodent from the montane forest of central eastern Madagascar (Muridae: Nesomyinae: Voalavo)

ABSTRACT A new species of rodent, Voalavo antsahabensis, from the eastern montane forest of Madagascar, is described from material obtained in the Anjozorobe region of the Central Highlands. The genus Voalavo was previously only known from the mountains of Anjanaharibe-Sud and Marojejy in the Northern Highlands. Several morphological, cranial, and dental characters separate V. antsahabensis from the only other named species in the genus, V. gymnocaudus. The recent discovery of this new taxon, after many years of survey work in the Anjozorobe Forest, has important implications for interpreting estimates of small mammal species richness and biogeographic patterns based on rapid inventories.

Patterns of morphological and molecular variation in Acrocephalus newtoni on Madagascar

Goodman, S.M., Tello, J.G. & Langrand, O. 2000. Patterns of mor-phological and biochemical variation in Acracephalus newtoni on Madagascar. Ostrich 71(3&4): 367-370. The endemic Madagascar Swamp-Warbler, Acrocephalus newtoni, generally occurs in lowland or upper mid-elevation (to c. 1800 m) aquatic habitats associated with slow-moving river, stagnant marshes and swamps in most regions of the island. In 1995, a population of swamp-warbler was found above tree-line in a dry ericoid zone of vegetation on the Andringitra Massif (at 2050 m) in south-central Madagascar, a very different habitat from that typically occupied by A. newtoni. Given the typical habitat specificity of members of the genus Acrocephalus, we expected the Andringitra birds to show differences at the specific level in comparison to marsh-dwelling A. newtoni. Using morphological and molecular characters it was found that the Andringitra population cannot be differentiated from typical A. newton.