Natural hybridization generates mammalian lineage with species characteristics

Abstract

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...

A separate lowstand lake at the northern edge of Lake Tanganyika? Evidence from phylogeographic patterns in the cichlid genus Tropheus

“…Under particular circumstances hybridization upon secondary contact might actually lead to a novel evolutionary stable entity, as, for example, suggested for a number of animal taxa (Grant & Grant, 2002;Gompert et al, 2006;Larsen et al, 2010;, including other cichlid fishes (Salzburger et al, 2002). It has been shown that hybrid populations can rapidly generate novel (''transgressive'') phenotypes which might be rapidly sorted out via natural selection, or alternatively, that hybrid populations become isolated from their sources in particular habitats, to form a novel entity distinct from both parental species (Salzburger et al, 2002;Parsons et al, 2011).…”

Is homoploid hybrid speciation that rare? An empiricist’s view

“…G Nieto Feliner, I Álvarez, J Fuertes-Aguilar, M Heuertz, I Marques, F Moharrek, R Piñeiro, R Riina, JA Rosselló, PS Soltis and I Villa-Machío Heredity (2017) 118, 513-516;doi:10.1038/hdy.2017published online 15 March 2017 N atural hybridization and its role in evolution and specifically in generating new diversity is an old and yet endlessly revitalized topic (Lotsy, 1916;Anderson, 1949;Stebbins, 1959;Rieseberg et al, 2003;Mallet, 2007;Soltis and Soltis, 2009;Larsen et al, 2010;Arnold et al, 2012b;Pereira et al, 2014;Grant and Grant, 2015;Abbott et al, 2016;Pennisi, 2016). Homoploid hybrid speciation (HHS) is the formation of a newhybrid-species, independent from its parents, via hybridization with no whole-genome duplication and thus no increase in ploidy.…”

Interpreting Large-Scale Phylogenetic Models of Mammal Class Diversification Based on Mitochondrial Biomarkers

“…I would also point out that examples of natural hybridization leading to speciation are exceedingly rare, especially in mammals Arnold et al, 1997 [13] . While most known cases of hybrid speciation occur in plants, the majority of documented cases involving animals have been observed in fish and insects Larsen et al, 2010 [26] . Perhaps most important in this discussion, mtDNA datasets have repeatedly shown to provide enough sufficient resolution for reconstructing a robust phylogeny and it also facilitates the molecular dating of divergence events within a phylogeny Krause et al, 2008 [27] .…”