The Caribbean slipper spurge Euphorbia tithymaloides: the first example of a ring species in plants

Abstract

A ring species arises when a parental population expands around an area of unsuitable habitat in such a way that when the two fronts meet they behave as distinct species while still being connected through a series of intergrading populations. Ring species offer great possibilities for studying the forces causing species divergence (e.g. the nature of pre-zygotic or post-zygotic reproductive isolation) or helping to maintain species integrity (e.g. reinforcement). Yet, ring species are extremely rare, and have only been documented convincingly in animals. Here, we present phylogenetic analyses of two nuclear gene regions from the Caribbean slipper spurge (Euphorbia tithymaloides) species complex that provide evidence that this group forms a ring species. These data show that the species complex originated in the area where Mexico and Guatemala meet, and expanded around the Caribbean basin along two distinct fronts: one eastward through the Yucatan Peninsula and into the Greater Antilles (GA); one southeastward through northern South America and then northward to the Lesser Antilles and eastern GA. The two terminal forms co-occur in the Virgin Islands and appear to be morphologically and ecologically distinct. Thus, our results suggest that Euphorbia tithymaloides is the first compelling example of a ring species in plants.

Figure 1.

According to the ring-species model, a parental population diverges along two fronts around an area of unsuitable habitat so that its terminal forms behave as distinct species upon secondary contact.

Figure 2.

Documented populations of E. tithymaloides in the Caribbean are represented in full circles, colour-coded by subspecies. The 42 populations included in this study are marked with an asterisk and have been assigned names representative of their localities.

Figure 3.

Two morphologically and ecologically distinct forms of E. tithymaloides coexist in the Greater Antilles. (a) E. t. ssp. angustifolia; (b) E. t. ssp. padifolia.

Figure 4.

ML allele tree for SGN. Tips represent alleles; only one allele is depicted for those individuals that are homozygous (oa), and both alleles (a1, a2) for heterozygotes (individuals of E. tithymaloides are diploid [15]). Support values correspond to posterior probability/ML bootstrap/MP bootstrap. Tips are colour coded by subspecies and abbreviations for the population name correspond to those on figure 2.

Figure 5.

Observed heterozygosity for subspecies of E. tithymaloides in the Caribbean. Subspecies tithymaloides Mex-C.Am includes Guanica (see the electronic supplementary material); padifolia includes St Croix. Correlation is significant at α = 0.05 (p = 0.01423). Excluding Vieques from the analysis yields a model significant at α = 0.1 (y = 1.0066x − 0.1618, R² = 0.5391, p = 0.09656).