Hybridization and Transgressive Evolution Generate Diversity in an Adaptive Radiation of Anolis Lizards

Abstract

Interspecific hybridization may act as a major force contributing to the evolution of biodiversity. Although generally thought to reduce or constrain divergence between 2 species, hybridization can, paradoxically, promote divergence by increasing genetic variation or providing novel combinations of alleles that selection can act upon to move lineages toward new adaptive peaks. Hybridization may, then, play a key role in adaptive radiation by allowing lineages to diversify into new ecological space. Here, we test for signatures of historical hybridization in the Anolis lizards of Puerto Rico and evaluate 2 hypotheses for the role of hybridization in facilitating adaptive radiation-the hybrid swarm origins hypothesis and the syngameon hypothesis. Using whole genome sequences from all 10 species of Puerto Rican anoles, we calculated D and f-statistics (from ABBA-BABA tests) to test for introgression across the radiation and employed multispecies network coalescent methods to reconstruct phylogenetic networks that allow for hybridization. We then analyzed morphological data for these species to test for patterns consistent with transgressive evolution, a phenomenon in which the trait of a hybrid lineage is found outside of the range of its 2 parents. Our analyses uncovered strong evidence for introgression at multiple stages of the radiation, including support for an ancient hybrid origin of a clade comprising half of the extant Puerto Rican anole species. Moreover, we detected significant signals of transgressive evolution for 2 ecologically important traits, head length and toepad width, the latter of which has been described as a key innovation in Anolis. [Adaptive radiation; introgression; multispecies network coalescent; phenotypic evolution; phylogenetic network; reticulation; syngameon; transgressive segregation.].

Figure 1.

Phylogeny of the Puerto Rican anoles reconstructed using ASTRAL (right) and phylogenetic network inferred using SNaQ and PhyloNet (left). Numbers above branches represent posterior probabilities on the phylogeny (right) and bootstrap support values on the phylogenetic network (left); numbers below branches on the phylogeny (right) indicate gene concordance factors. For the phylogenetic network, blue branches represent inferred reticulations. The numbers above the bars next to these branches indicate bootstrap support values from the SNaQ analysis; the numbers below the bars represent the ancestry proportions (γ) inferred by SNaQ. The asterisk (*) identifies the reticulation that received bootstrap support (>70) in the PhyloNet analysis.

Figure 2.

Heatmap for pairwise f-branch (f_b) statistics calculated using Dsuite (Dalquen et al. 2017). The f_b statistic represents excess sharing of derived alleles between the branch of the tree on the y-axis (left) and the species on the x-axis (top). Darker colors indicate higher f_b values, and asterisks (*) indicate values that were significantly elevated after Holm-Bonferroni correction (FWER < 0.001). Individual f_b scores are listed in Supplementary Table S3.