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The origin of the parrotfish species Scarus compressus in the Tropical Eastern Pacific: region-wide hybridization between ancient species pairs

Citation

Carlon, David et al. (2020), The origin of the parrotfish species Scarus compressus in the Tropical Eastern Pacific: region-wide hybridization between ancient species pairs, Dryad, Dataset, https://doi.org/10.5061/dryad.jwstqjq69

Abstract

Background: An increasing number of hybrid zones with varying evolutionary outcomes have been documented from different reef fish families. In the Tropical Eastern Pacific (TEP), four species of parrotfishes occur in sympatry on rocky reefs from Baja California to Ecuador: Scarus. compressus,S. ghobbanS. perrico, and S. rubroviolaceus; and have complex phylogeographic histories. The most divergent,S. perrico, belongs to a Tropical American clade that diverged from a Central Indo-Pacific ancestor in the late Miocene (6.6 Ma). We tested the hypothesis that S. compressuswas the result of ongoing hybridization among the other three species by sequencing four nuclear markers and a mitochondrial locus in samples spanning 2/3 of the latitudinal extent of the TEP. 

Results: A structure model of all samples indicated that K=3 was the best fit to the nuclear data and that individuals identified as S. compressushad admixed assignment values (Q). Power analyses indicated our data could correctly detect and assign pure adults and F1 hybrids with > 0.90 probability, and correct assignment of F2 was also high in some cases. NewHybrids models revealed that 89.8% (n= 59) of the Scarus compressus samples were F1 hybrids of crosses between divergent species pairs: S. perrico × S. ghobbanand S. perrico × S. rubroviolaceus. Similarly, S.ghobban and S. rubroviolaceuswere also hybridizing, with ½ of the admixed individuals assigned to F1 hybrids and the remainder likely deep generation hybrids. We observed strong mito-nuclear discordance in all three hybrid pairs, but found little evidence for accelerated mt vs. nuclear evolution in the paternal species. Bayesian analysis of Migrate models favours gene flow between S. perricoand S. ghobban, but not other species pairs. 

Conclusions: Mating between species whose ancestors diverged in the late Miocene is giving rise to region wide, hybrid complex, characterized by a high frequency of parental and F1 genotypes but a low frequency of deep generation hybrids. Trimodal structure, combined with reproductive evidence for fertility of both male and female F1 hybrids, suggest that fitness declines sharply in later generation hybrids. In contrast, the hybrid population of the two younger species had similar frequencies of F1 and > F1 hybrids. These differences are consistent with a model of accelerating post-mating incompatibility with time. Mitochondrial genotypes in hybrids, suggests indiscriminate mating by male S. perricois driving pre-zygotic breakdown, which may reflect the isolation of this endemic species in the TEP for millions of years and weak selection for conspecific mate recognition. Despite overlapping habitat use, high rates of hybridization, and evidence for historical gene flow, species boundaries are maintained by post-mating processes in this complex.