Madagascar's Central Highlands are largely composed of grasslands, interspersed with patches of forest. The historical perspective was that Madagascar's grasslands had anthropogenic origins, but emerging evidence suggests that grasslands were a component of the pre-human Central Highlands vegetation. Consequently, there is now vigorous debate regarding the extent to which these grasslands have expanded due to anthropogenic pressures. Here, we shed light on the temporal dynamics of Madagascar's vegetative composition by conducting a population genomic investigation of Goodman's mouse lemur (Microcebus lehilahytsara; Cheirogaleidae). These smallbodied primates occur both in Madagascar's eastern rainforests and in the Central Highlands, making them a valuable indicator species. Population divergences among forest-dwelling mammals will reflect changes to their habitat, including fragmentation, whereas patterns of post-divergence gene flow can reveal formerly wooded migration corridors. To explore these patterns, we used RADseq data to infer population genetic
Madagascar’s Central Highlands are largely composed of grasslands,
interspersed with patches of forest. The pre-human extent of these
grasslands is a topic of vigorous debate, with conventional wisdom
holding that they are anthropogenic in nature and emerging evidence
supporting that grasslands were a component of the pre-human Central
Highlands vegetation. Here, we shed light on the temporal dynamics of
Madagascar’s vegetative composition by conducting a population genomic
investigation of Goodman’s mouse lemur (Microcebus lehilahytsara;
Cheirogaleidae). These small-bodied primates occur both in Madagascar’s
eastern rainforests and in the Central Highlands, which makes them a
valuable indicator species. Population divergences among forest-dwelling
mammals can serve as a proxy for habitat fragmentation and patterns of
post-divergence gene flow can reveal potential migration corridors
consistent with a wooded grassland mosiac. We used RADseq data to infer
phylogenetic relationships, population structure, demographic models of
post-divergence gene flow, and population size change through time.
These analyses offer evidence that open habitats are an ancient
component of the Central Highlands, and that wide-spread forest
fragmentation occurred naturally during a period of decreased
precipitation near the last glacial maximum. Models of gene flow suggest
that migration across the Central Highlands has been possible from the
Pleistocene through the recent Holocene via riparian corridors. Notably,
though our findings support the hypothesis that Central Highland
grasslands predate human arrival, we also find evidence for
human-mediated population declines. This highlights the extent to which
species imminently threatened by human-mediated deforestation may be
more vulnerable from paleoclimatic changes.
The occurrence of natural hybridization has been reported in a wide range of organisms, including primates. The present study focuses on the endemic lemurs of Madagascar, primates for which only a few species occur in sympatry or parapatry with congeners, thereby creating limited opportunity for natural hybridization. This study examines RADseq data from 480 individuals to investigate whether the recent expansion of Microcebus murinus towards the northwest and subsequent secondary contact with Microcebus ravelobensis has resulted in the occurrence of hybridization between the two species. Admixture analysis identified one individual with 26% of nuclear admixture, which may correspond to an F2- or F3-hybrid. A composite-likelihood approach was subsequently used to test the fit of alternative phylogeographic scenarios to the genomic data and to date introgression. The simulations yielded support for low levels of gene flow (2Nm0 = 0.063) between the two species starting before the Last Glacial Maximum (between 54 and 142 kyr). Since M. murinus most likely colonized northwestern Madagascar during the Late Pleistocene, the rather recent secondary contact with M. ravelobensis has likely created the opportunity for occasional hybridization. Although reproductive isolation between these distantly related congeners is not complete, it is effective in maintaining species boundaries.
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