Hybridization and rapid differentiation after secondary contact between the native green anole (Anolis carolinensis) and the introduced green anole (Anolis porcatus)

Abstract

In allopatric species, reproductive isolation evolves through the accumulation of genetic incompatibilities. The degree of divergence required for complete reproductive isolation is highly variable across taxa, which makes the outcome of secondary contact between allopatric species unpredictable. Since before the Pliocene, two species of Anolis lizards, Anolis carolinensis and Anolis porcatus , have been allopatric, yet this period of independent evolution has not led to substantial species‐specific morphological differentiation, and therefore, they might not be reproductively isolated. In this study, we determined the genetic consequences of localized, secondary contact between the native green anole, A. carolinensis , and the introduced Cuban green anole, A. porcatus , in South Miami. Using 18 microsatellite markers, we found that the South Miami population formed a genetic cluster distinct from both parental species. Mitochondrial DNA revealed maternal A. porcatus ancestry for 35% of the individuals sampled from this population, indicating a high degree of cytonuclear discordance. Thus, hybridization with A. porcatus , not just population structure within A. carolinensis , may be responsible for the genetic distinctiveness of this population. Using tree‐based maximum‐likelihood analysis, we found support for a more recent, secondary introduction of A. porcatus to Florida. Evidence that ~33% of the nuclear DNA resulted from a secondary introduction supports the hybrid origin of the green anole population in South Miami. We used multiple lines of evidence and multiple genetic markers to reconstruct otherwise cryptic patterns of species introduction and hybridization. Genetic evidence for a lack of reproductive isolation, as well as morphological similarities between the two species, supports revising the taxonomy of A. carolinensis to include A. porcatus from western Cuba. Future studies should target the current geographic extent of introgression originating from the past injection of genetic material from Cuban green anoles and determine the consequences for the evolutionary trajectory of green anole populations in southern Florida.

The identity of the introduced green anole (Reptilia: Squamata) of Hawaii and other Pacific islands

“…The situation of A. carolinensis in southern Florida is complicated by the presence of introduced A. porcatus (Powell et al 2016, Krysko et al 2019). Both of these sets of authors state that there are no morphological differences between the native and introduced form and that they interbreed (as confirmed by Wegener et al 2019) In stating that there are no morphological differences between Anolis carolinensis and A. porcatus, Krysko et al (2019) explicitly relied upon the work of Camposano (2011). The latter author showed that A. carolinensis-group anoles in Miami-Dade County in southern Florida cannot be separated into two distinct moieties corresponding to A. carolinensis and A. porcatus.…”

“…2). The great morphological variation in Miami-Dade County doubtless results from the introduction of A. porcatus and subsequent interbreeding (Kolbe et al 2007, Wegener et al 2019 with A. carolinensis.…”

“…The status of Anolis porcatus.-Although the situation of Anolis porcatus in Cuba needs further study, Glor et al (2005) showed that A. carolinensis originated from within the western lineage of A. porcatus. Kolbe et al (2007) and Wegener et al (2019) have shown that the introduced A. porcatus in southeastern Florida have interbred to a considerable extent with the native A. carolinensis. The latter state that they are ''not reproductively isolated and interbreed successfully after secondary contact, leading to a fusion of the previously distinct lineages''; Wegener et al (2019:4144-4145) conclude that the western lineage of A. porcatus ''should be subsumed into the earlier named A.…”

Natural hybridization between two species of green Anoles: morphological and genetic evidence

“…The fact that only a few reports on anoles hybridization exist (e.g., Gorman & Atkins, 1968;Glor et al, 2004;Kӧhler et al, 2010;Jezcova et al, 2013;Wegener et al, 2019) and even fewer reports on interspecific mating (e.g., Arias, 1985), might be interpreted as evidence of the existence of good reproductive isolating mechanisms, but could also be interpreted as a lack of combined genetic and morphologic investigations. (Schenk et al, 2008).…”

Rapid evolutionary divergence of a songbird population following recent colonization of an anthropogenic habitat

“…Moreover, moderate admixture can also contribute to colonization success by minimizing deleterious effects of reduced intra-population diversity or by introducing favorable alleles and enhancing evolutionary potential (Keller & Taylor 2010). That introgression between taxa contributes to adaptation and sorting of genes has become increasingly recognized as a major contributor to population divergence and speciation (Abbott et al 2013;Lamichhaney et al 2015;Wegener et al 2019). Based on our genomic analyses and on the migration rates reported here and in Yeh and Price (2004), as well as in the phenotypic studies in Yeh (2004), it seems that several over-wintering birds on the UCSD campus came from populations other than pinosus , and some of these may have remained to breed on campus.…”