Most diploid species arise from single-species ancestors. Hybrid origins of new species are uncommon (except among polyploids) and are documented infrequently in animals. Examples of natural hybridization leading to speciation in mammals are exceedingly rare. Here, we show a Caribbean species of bat (Artibeus schwartzi) has a nuclear genome derived from two nonsister but congeneric species (A. jamaicensis and A. planirostris) and a mitochondrial genome that is from a third extinct or uncharacterized congener. Artibeus schwartzi is self-sustaining, morphologically distinct, and exists in near geographic isolation of its known parent species. Island effects (i.e., area, reduced habitat variability, and geographic isolation) likely have restricted gene flow from parental species into the Caribbean populations of this hybrid lineage, thus contributing to local adaptation and isolation of this newly produced taxon. We hypothesize differential rates of the development of reproductive isolation within the genus and estimate that 2.5 million years was an insufficient amount of time for the development of postzygotic isolation among the three species that hybridized to produce A. schwartzi. Reticulated evolution thus has resulted in a genomic combination from three evolutionary lineages and a transgressive phenotype that is distinct from all other known species of Artibeus. The data herein further demonstrate the phenomenon of speciation by hybridization in mammals is possible in nature.Artibeus | Chiroptera | hybrid speciation | reticulate evolution | transgressive segregation D espite empirical studies documenting the establishment of animal hybrid lineages (1-8), the evolutionary importance of speciation by natural hybridization in animals is unknown and often is considered minor because the offspring of such crosses typically are less fit than either parental species (9, 10). Nearly all reported cases of homoploid speciation events (hybrid speciation without change in chromosome number) (11) in animals are among species of insects or fish (12), and there are only a handful of suspected cases in mammals (13-17). Thus hybrid speciation appears to be especially rare in mammals, a consequence of either unfavorable conditions for hybrid speciation to occur (i.e., ecological, physiological, hybrid zone structure) or a lack of empirically based research (18,19). Here, we describe a zone of admixture on a series of Caribbean islands within which three species of Neotropical bats have hybridized resulting in a novel lineage with species-level distinction. Our genetic and morphometric analyses have identified a unique hybrid zone among species of fruit-eating bats, leading us to the hypothesis that natural hybridization has generated a distinct lineage that exists in these insular populations. Our data also indicate that this phenotypic and genotypic combination is geographically isolated from extant parental species on the southern Lesser Antillean island of Saint Vincent.Two species of fruit-eating bats, Artibeus jamaicensis...

Population divergence is the first step in allopatric speciation, as has long been recognized in both theoretical models of speciation and empirical explorations of natural systems. All else being equal, lineages with substantial population differentiation should form new species more quickly than lineages that maintain range-wide genetic cohesion through high levels of gene flow. However, there have been few direct tests of the extent to which population differentiation predicts speciation rates as measured on phylogenetic trees. Here, we explicitly test the links between organismal traits, population-level processes, and phylogenetic speciation rates across a diverse clade of Australian lizards that shows remarkable variation in speciation rate. Using genome-wide double digest restriction site-associated DNA data from 892 individuals, we generated a comparative data set on isolation by distance and population differentiation across 104 putative species-level lineages (operational taxonomic units). We find that species show substantial variation in the extent of population differentiation, and this variation is predicted by organismal traits that are thought to be proxies for dispersal and deme size. However, variation in population structure does not predict variation in speciation rate. Our results suggest that population differentiation is not the rate-limiting step in species formation and that other ecological and historical factors are primary determinants of speciation rates at macroevolutionary scales.

Understanding the spatial distribution of phenotypes and their association with local environmental conditions can provide important insights into the evolutionary history and ecological dynamics of species. Geographical variation in the skull size of the Artibeus lituratus complex was explored to evaluate the association between morphological traits and habitat-specific environmental conditions in the mainland populations of Middle and South America. We performed a principal component analysis based on 390 museum specimens using 17 cranial and mandibular measurements to explore the overall morphometric variation in our sample. Additionally, we used the information from 19 bioclimatic variables from 127 collecting localities to assess the extent of variation in environmental space across our study area. A canonical correlation analysis performed to evaluate the association between morphological and environmental variables indicated a high correlation between morphology and environment. Seasonality was correlated with skull size (canonical r = 0.7). Specifically, skull size in the A. lituratus complex increases as the amount of precipitation during the driest season increases and as inter-annual precipitation variability decreases. This result supports the hypothesis that environmental pressures are at least partially responsible for the skull size differences observed. Moreover, the nonrandom distribution of individuals with different skull sizes suggests that environmental filtering plays a role in determining the geographical distribution of morphological variants.

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