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.

Fig. 1.

Neotropical distributions and admixture among Caribbean species of Artibeus. (Left) A. jamaicensis is restricted to west of the Andes Mountains in South America. A. planirostris is distributed throughout much of South America east of the Andes Mountains. Both species recently have come into primary contact in the southern Lesser Antilles. Inset shows mtDNA haplotype frequencies at the region of primary contact (St. Lucia: n = 48; St. Vincent: n = 126; Grenadines: n = 48; Grenada: n = 33). (Right) Results of a structure analysis of 218 AFLP fragments reveals admixture between the nuclear genomes of A. jamaicensis and A. planirostris in southern Lesser Antillean populations. Sampled populations for AFLP analyses included (1) A. jamaicensis: Central America and Jamaica, (2) A. jamaicensis, A. schwartzi, and A. planirostris: St. Lucia, St. Vincent and the Grenadines, and Carriacou Island, and (3) A. planirostris: Grenada, Venezuela, and Ecuador.

Fig. 2.

Mitochondrial (cyt-b) and nuclear (AFLP) phylogenies of species of Artibeus examined herein and results of a homoplasy excess test performed on AFLP data. (A) Cyt-b and AFLP phylograms showing species-level variation within the genus. Clades A–F identify ingroup species-level clusters of the AFLP dataset. Arrow indicates the change in topology with addition of individuals from the southern Lesser Antilles. (B) Results of a homoplasy excess test of 374 AFLP fragments. The y axis identifies basal nodes for each species indicated in A, and the x axis represents bootstrap support values of 1,000 iterations. Removal of putative hybrid taxa increased bootstrap support values for A. jamaicensis (clade F) and A. planirostris (clade E) to 91% and 95%, respectively (black dots). Solid lines indicate 100% bootstrap support values for clades A and C in all analyses.

Fig. 3.

Transgressive segregation by Artibeus schwartzi. Results of a PCA on 17 cranial and mandibular measurements of A. jamaicensis, A. planirostris, and A. schwartzi collected from throughout the Caribbean. Within A. schwartzi: ●, specimens collected from St. Vincent (SV); ○, specimens collected from St. Lucia (SL) and the Grenadines (G) (Fig. 1). Descriptive statistics and factor loadings are presented in Tables S3 and S4.

Fig. 4.

Timescale of diversification of Artibeus. Chronogram depicts diversification of four species of Dermanura and 12 species of Artibeus based on complete cyt-b sequences. Nonreproductively isolated taxa (A. jamaicensis, A. planirostris, A. schwartzi) are in bold. TMRCA for these species was estimated at ~2.5 Mya. Gray bars indicate 95% highest posterior density for divergence estimates. *, Unrecognized species-level variation in Brazil (26). The timescale of diversification presented here is compatible with major paleogeographic events in the Neotropics: the split between Central American endemics (A. inopinatus, A. hirsutus) and the remainder of the genus coincides with the closure of the Panamanian Isthmus (~3.5 Mya) (39); the split between A. hirsutus and A. fraterculus (a southwestern Andean endemic) occurs subsequent to the closure of the Panamanian Isthmus; the split between the A. jamaicensis complex (distributed west of the Andes Mountains) and the remainder of the genus is compatible with isolation resulting from uplifts of the Andean chain (from ~5 Mya to present) (40).