Multiple nuclear loci reveal patterns of incomplete lineage sorting and complex species history within western mouse lemurs (Microcebus)

Mouse lemurs (genus Microcebus) are nocturnal primates endemic to the island of Madagascar. Until recently, they were classified as two species, one from eastern and one from western Madagascar. Previously published analyses of morphometric and mitochondrial DNA data show strong support for the recognition of more than eight species, however. Here, we test the eight-species hypothesis with DNA data derived from four independently segregating nuclear loci. We find many areas of congruence between the mitochondrial and nuclear data, but incomplete lineage sorting and low mutation rates limit the phylogenetic resolution of the nuclear data. Even so, the nuclear loci unanimously find evidence for three deeply diverged lineages within the mouse lemur radiation: one that is congruent with the mtDNA "southern clade", another that is congruent with the mtDNA "northern clade", and one monospecific branch comprised of the species Microcebus ravelobensis. The latter result in particular emphasizes the need for careful biological study of this species.     

Genetic Differentiation and Demographic History of the Northern Rufous Mouse Lemur (<Emphasis Type="Italic">Microcebus tavaratra</Emphasis>) Across a Fragmented Landscape in Northern Madagascar

Phylogeographic barriers, together with habitat loss and fragmentation, contribute to the evolution of a species’ genetic diversity by limiting gene flow and increasing genetic differentiation among populations. Changes in connectivity can thus affect the genetic diversity of populations, which may influence the evolutionary potential of species and the survival of populations in the long term. We studied the genetic diversity of the little known Northern rufous mouse lemur (Microcebus tavaratra), endemic to Northern Madagascar. We focused on the population of M. tavaratra in the Loky–Manambato region, Northern Madagascar, a region delimited by two permanent rivers and characterized by a mosaic of fragmented forests. We genotyped 148 individuals at three mitochondrial loci (D-loop, cytb, and cox2) in all the major forests of the study region. Our analyses suggest that M. tavaratra holds average genetic diversity when compared to other mouse lemur species, and we identified two to four genetic clusters in the study region, a pattern similar to that observed in another lemur endemic to the region (Propithecus tattersalli). The main cluster involved samples from the two mountain forests in the study region, which were connected until recently. However, the river crossing the study region does not appear to be a strict barrier to gene flow in M. tavaratra. Finally, the inferred demographic history of M. tavaratra suggests no detectable departure from stationarity over the last millennia. Comparisons with codistributed species (P. tattersalli and two endemic rodents, Eliurus spp.) suggest both differences and similarities in the genetic clusters identified (i.e., barriers to species dispersal) and in the inferred demographic history. These comparisons suggest that studies of codistributed species are important to understand the effects of landscape features on species and to reconstruct the history of habitat changes in a region.     

Female dominance in captive gray mouse lemurs (Microcebus murinus)

Female dominance or female feeding priority seem to be characteristic for many lemur species, but are rare traits in other primates and mammals in general. The nocturnal lemur species, however, are underrepresented in the quantitative studies on social dominance. The aim of this study is to investigate the pattern of intersexual dominance relationships in the gray mouse lemur (Microcebus murinus), a species that is generally thought to possess a number of ancestral lemur traits. The context, distribution, and outcome of intersexual conflicts are analyzed in four captive groups of gray mouse lemurs. Intersexual conflicts occurred in the study groups in different behavioral contexts and were mostly spatial interactions (chasing/fleeing, approach/avoidance). The majority of conflicts were decided, and were in all but one case won by females. This is the first evidence suggesting unconditional female dominance in a cheirogaleid primate. The existence of female dominance in most families of the Lemuriformes suggests it is an ancient trait that evolved in their common ancestor.     

Test of Fox's assembly rule for functional groups in lemur communities in Madagascar

This paper examines to what extent an assembly rule designed by Fox for small terrestrial mammal communities is also applicable to communities of arboreal lemurs in Madagascar. This approach extends the testing of Fox's assembly rule to a new biogeographic region and a different phylogenetic radiation. The rule operates on a functional rather than on the taxonomic level. It specifies that: "There is a much higher probability that each species entering a community will be drawn from a different functional group, until each group is represented before the cycle repeats" (Fox, 1987: 201). This rule was tested with lemur communities from 14 sites in evergreen rain forests and nine sites in dry deciduous forests of Madagascar. Lemur species were assigned to one of three different functional groups based on dietary preferences: omnivores, frugivores, folivores. The rule applies almost perfectly to extant lemur communities in evergreen rain forest. Present communities in dry deciduous forests are not ordered as perfectly as communities of the rain forest sites, but they also deviate from random assembly as generated by the null model. Including extinct species of the dry forest ecosystem indicates that the at present unfavoured composition of the lemur community has been derived from a favoured state through extinction of the large folivorous and frugivorous lemur species. In the lemur communities of the eastern Malagasy rain forest, the assembly went through at least four, and in the Holocene dry forest ecosystem through even five, cycles without failing. This assigns considerable significance to the underlying mechanisms (most likely interspecific competition) and indicates that they are still effective in the forests of Madagascar. The dry deciduous forests might have been subject to recent natural and anthropogenic changes which interfere with the operation of these deterministic processes.     

A biogeographical perspective on the variation in mouse lemur density throughout Madagascar

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Aspects of reproduction in the eastern rufous mouse lemur (Microcebus rufus) and their implications for captive management

The eastern rufous mouse lemur is one of the smallest primate species. It inhabits the eastern rain forest of Madagascar. Its reproductive biology has not been examined because of its rarity in laboratories. We present the first data on reproduction and variation in reproductive success from a breeding colony of wild‐caught Microcebus rufus. The eastern rufous mouse lemur shows a seasonal change in testicular size and in the occurrence of estrus. Females had 2.5 cycles (range, one to four) per season. The estrous cycle length was 59 days (range, 51–66), the duration of vaginal opening during estrus was 7.5 days (range, 5–8), receptivity occurred on the third day of estrus, gestation length was 56.5 days (range, 56–57), litter size was two neonates (range, one to three). The frequency and duration of mating behavior varied widely among the pairs. Copulation seemed to occur on a single day per estrus within the first to fourth hour after light change to red light. In four cases (three pairs), copulation lasted between 15 and 240 seconds. Breeding success can be increased by choosing mates carefully. Microcebus rufus seems to be a seasonal breeder like its sibling species Microcebus murinus. In wild‐caught animals, males seemed to adapt quickly (first season) to the conditions of captivity, whereas in the females, individual variation (first to third season) in reproductive activity was observed. Air humidity of >60% seems to facilitate the breeding success in wild‐caught pairs. First pregnancy and successful rearing of offspring occurred in the second and fourth year of captivity in two of three females. Wild‐caught eastern rufous mouse lemurs seemed to demonstrate variation in adapting to the conditions of captivity with regard to sex and individuality. Zoo Biol 20:157–167, 2001. © 2001 Wiley‐Liss, Inc.     

A New Species of Megophryid Frog of the Genus Scutiger from Kangchenjunga Conservation Area,Eastern Nepal

This study investigated the systematics of the megophryid genus Scutiger from eastern and western Nepal using molecular and morphological data. Our results support two divergent lineages, one of which has nuptial spines on the dorsal surface of the first three fingers while the other has spines only on the dorsal surface of the first two fingers. The Ghunsa lineage from eastern Nepal shows significant morphological and molecular differences to other species of genus Scutiger and is here described as a new species. Based on the molecular analysis, the Muktinath lineage from western Nepal is confirmed to be Scutiger boulengeri and represents a species complex widespread throughout the Himalayan region. The newly described taxon is endemic to the eastern Himalayas and currently known only from the Ghunsa valley, Taplejung district, Nepal.     

Food partitioning among Malagasy primates

Summary Food partitioning among lemurs was studied in relation to food patch size and plant chemistry in the eastern rainforest and a western deciduous forest of Madagascar. Patch size (i.e. crown diameter of food trees) is significantly correlated with group body weight of different lemur species. But intraspecific variability is high and prevents effective species separation. Chemical analyses of more than 400 plant parts eaten by seven different lemur species revealed major differences in their food choice with respect to protein concentrations, condensed tannins and alkaloids. Among the leaf eating lemurs discriminant analysis segregates three groups à two species based on chemical characteristics of their food. Whereas differences in food chemistry are pronounced between groups they are lacking between the two species within each group. The two species of each group avoid interference competition by different activity rhythms. Actual competition for slowly renewable resources such as leaves and fruit, however, can not be reduced by different activities. Here interspecific differences in gross categories of food, food species composition and different habitat utilization due to other constraints may contribute to the possible coexistence of species. Thus interspecific differences in food selection in relation to primary and secondary plant chemicals is an integrated part of the mechanisms allowing several primate species to coexist in sympatry.     

Conservation and genetics of the frosted flatwoods salamander (Ambystoma cingulatum) on the Atlantic coastal plain

The federally threatened frosted flatwoods salamander, Ambystoma cingulatum, occurs in isolated populations on the coastal plain of northern Florida, Georgia and South Carolina. An earlier phylogeographic study based primarily on mitochondrial DNA (mtDNA) and morphometrics demonstrated that the previously recognized species A. cingulatum contained two cryptic species, and that two distinct mtDNA clades were contained within the newly restricted A. cingulatum. However, salamanders from the northern extent of the species range in South Carolina were not previously available for analysis. Here, we used individuals from a newly discovered South Carolina breeding site to determine whether A. cingulatum from South Carolina are genetically distinct from their more southerly conspecifics. These analyses included the mitochondrial gene studied previously as well as broad geographic sampling of three rapidly evolving nuclear genes that allowed us to further investigate lineage diversification of flatwoods salamanders. The mitochondrial and nuclear results are largely congruent, yielding strong support for two distinct species of flatwoods salamanders and also two lineages within the eastern species. Further, the South Carolina specimens are closely related to other haplotypes found in eastern Georgia and Florida. Our summary of field surveys over the past 20 years indicates that this South Carolina population may be one of only three remaining in the entire Atlantic coastal plain distribution of this rare and declining amphibian species.     

Forest Type Influences Population Densities of Nocturnal Lemurs in Manompana,Northeastern Madagascar

Forest loss, fragmentation, and anthropization threaten the survival of forest species all over the world. Shifting agriculture is one of these threatening processes in Madagascar. However, when its cycle is halted and the land is left to regenerate, the resulting growth of secondary forest may provide a viable habitat for folivorous and omnivorous lemur species. We aimed to identify the response of nocturnal lemurs to different successional stages of regenerating secondary, degraded mature, and mature forest across a mosaic-type landscape. We surveyed four nocturnal lemur species (Avahi laniger, Microcebus cf. simmonsi, Allocebus trichotis, and Daubentonia madagascariensis) in four forest types of varying habitat disturbance in northeastern Madagascar. We estimated densities in mature and regenerating secondary forest for the eastern woolly lemur (Avahi laniger) and mouse lemur (Microcebus cf. simmonsi), two sympatric species with folivorous and omnivorous diets respectively. We did not estimate densities of Allocebus trichotis and Daubentonia madagascariensis owing to small sample size; however, we observed both species exclusively in mature forest. We found higher population densities of A. laniger and M. cf. simmonsi in secondary than in mature forest, showing the potential of regenerating secondary forest for lemur conservation. Several environmental factors influenced the detectability of the two lemur species. While observer and habitat type influenced detection of the eastern woolly lemur, canopy height and vine density influenced detection of mouse lemurs. Understanding how different species with different diets interact with anthropogenically impacted habitat will aid future management decisions for the conservation of primate species.     

Evidence of prolonged torpor in Goodman’s mouse lemurs at Ankafobe forest,central Madagascar

The small-bodied mouse lemurs of Madagascar (Microcebus) are capable of heterothermy (i.e., torpor or hibernation). The expression of these energy-saving strategies has been physiologically demonstrated in three species: M. berthae, the pygmy mouse lemur (daily torpor), M. murinus, the gray mouse lemur (daily torpor and hibernation), and M. griseorufus, the reddish-gray mouse lemur (daily, prolonged torpor and hibernation). Additional evidence, based on radiotracking and seasonal body mass changes, indicated that mouse lemur capabilities for heterothermy extended to M. lehilahytsara, the Goodman’s mouse lemur. In this study, we confirm the use of hibernation in Goodman’s mouse lemurs at a new location, a high-plateau forest fragment in Ankafobe, central Madagascar. Our evidence is based on sleeping site monitoring of radiocollared individuals and the retrieval of three mouse lemurs from inside a tree hole, all of which displayed a lethargic state. Though our data are preliminary and scant, we show that hibernation occurs in high-plateau mouse lemurs, and suggest that a buffered environment (i.e., tree holes instead of nests) may be crucial to avoiding potentially extreme ambient temperatures.     

Frugivory in four sympatric lemurs: implications for the future of Madagascar's forests

Although some conservationists accept that not all species can be saved, we illustrate the difficulty in deciding which species are dispensable. In this article, we examine the possibility that the integrity of a forest relies on its entire faunal assemblage. In Madagascar, one faunal group, the lemurs, accounts for the greatest biomass and species richness among frugivores. For example, 7 of the 13 sympatric lemur species in Madagascar's eastern rainforests consume primarily fruit. Because of this, we suggest that some tree species may rely heavily on particular lemur taxa for both seed dispersal and germination. In Ranomafana National Park, the diets for four of the day-active lemur frugivores have been documented during annual cycles over a 5-year period. We predicted that, although the fruit of some plant taxa would be exploited by multiple lemur species, the fruit of others would be eaten by one lemur species alone. Analyses reveal that while lemurs overlap in a number of fruit taxa exploited, 46% (16/35) of families and 56% (29/52) of genera are eaten exclusively by one lemur species. We, therefore, predict local changes in forest composition and structure if certain of these lemur species are eliminated from a forest owing to hunting, disease, or habitat disturbance. We also suggest that this result may be of global significance because carbon sequestration by the tropical forests in Madagascar may be reduced as a result of this predicted change in forest composition.     

Phylogeny and biogeography of the genus Ainsliaea (Asteraceae) in the Sino-Japanese region based on nuclear rDNA and plastid DNA sequence data

BACKGROUND AND AIMS: The flora of the Sino-Japanese plant region of eastern Asia is distinctively rich compared with other floristic regions in the world. However, knowledge of its floristic evolution is fairly limited. The genus Ainsliaea is endemic to and distributed throughout the Sino-Japanese region. Its interspecific phylogenetic relationships have not been resolved. The aim is to provide insight into floristic evolution in eastern Asia on the basis of a molecular phylogenetic analysis of Ainsliaea species. METHODS: Cladistic analyses of the sequences of two nuclear (ITS, ETS) and one plastid (ndhF) regions were carried out individually and using the combined data from the three markers. KEY RESULTS: Phylogenetic analyses of three DNA regions confirmed that Ainsliaea is composed of three major clades that correspond to species distributions. Evolution of the three lineages was estimated to have occurred around 1.1 MYA during the early Pleistocene. CONCLUSIONS: The results suggest that Ainsliaea species evolved allopatrically and that the descendants were isolated in the eastern (between SE China and Japan, through Taiwan and the Ryukyu Islands) and western (Yunnan Province and its surrounding areas, including the Himalayas, the temperate region of Southeast Asia, and Sichuan Province) sides of the Sino-Japanese region. The results suggest that two distinct lineages of Ainsliaea have independently evolved in environmentally heterogeneous regions within the Sino-Japanese region. These regions have maintained rich and original floras due to their diverse climates and topographies.