Abstract
BackgroundIn the Tropical Eastern Pacific (TEP), four species of parrotfishes with complex phylogeographic histories co-occur in sympatry on rocky reefs from Baja California to Ecuador: Scarus compressus, S. ghobban, S. perrico, and S. rubroviolaceus. The most divergent, S. perrico, separated from a Central Indo-Pacific ancestor in the late Miocene (6.6 Ma). We tested the hypothesis that S. compressus was 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.ResultsA Structure model indicated that K = 3 fit the nuclear data and that S. compressus individuals had admixed genomes. Our data could correctly detect and assign pure adults and F1 hybrids with > 0.90 probability, and correct assignment of F2s was also high in some cases. NewHybrids models revealed that 89.8% (n = 59) of the S. compressus samples were F1 hybrids between either S. perrico × S. ghobban or S. perrico × S. rubroviolaceus. Similarly, the most recently diverged S. ghobban and S. rubroviolaceus were hybridizing in small numbers, with half of the admixed individuals assigned to F1 hybrids and the remainder likely > F1 hybrids. We observed strong mito-nuclear discordance in all hybrid pairs. Migrate models favored gene flow between S. perrico and S. ghobban, but not other species pairs.ConclusionsMating between divergent species is giving rise to a region-wide, multispecies hybrid complex, characterized by a high frequency of parental and F1 genotypes but a low frequency of > F1 hybrids. Trimodal structure, and 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 more recently diverged species had similar frequencies of F1 and > F1 hybrids, suggesting accelerating post-mating incompatibility with time. Mitochondrial genotypes in hybrids suggest that indiscriminate mating by male S. perrico is driving pre-zygotic breakdown, which may reflect isolation of this endemic species for millions of years resulting in weak selection for conspecific mate recognition. Despite overlapping habitat use and high rates of hybridization, species boundaries are maintained by a combination of pre- and post-mating processes in this complex.
Highlights
In the Tropical Eastern Pacific (TEP), four species of parrotfishes with complex phylogeographic histo‐ ries co-occur in sympatry on rocky reefs from Baja California to Ecuador: Scarus compressus, S. ghobban, S. perrico, and S. rubroviolaceus
We found that in both the S. ghobban × S. rubroviolaceus and the S. perrico × S. rubroviolaceus crosses, backcrosses occasionally had Q values that fell below the filtering threshold (Additional file 1: Figure S3)
Our data strongly support a hypothesis of contemporary hybridization between S. perrico × S. ghobban and S. perrico × S rubroviolaceus as an explanation for the phenotypes described as the species S. compressus in the TEP
Summary
In the Tropical Eastern Pacific (TEP), four species of parrotfishes with complex phylogeographic histo‐ ries co-occur in sympatry on rocky reefs from Baja California to Ecuador: Scarus compressus, S. ghobban, S. perrico, and S. rubroviolaceus. Hybridization has been documented in an increasing number of plant and animal systems [1] and has important consequences for evolutionary processes. At the macro-evolutionary level, hybridization and subsequent successful mating can result in transgressive segregation of unique traits [9, 10], producing novel phenotypes that may give rise to new species [11]. This process can spark adaptive radiation when highly divergent lineages hybridise and increase intraspecific variation in traits that facilitate diversification into vacant ecological niches [12, 13]. Understanding the ecological and genomic contexts that facilitate these divergent evolutionary scenarios calls for a broader systematic understanding of hybridization in the wild from a variety of empirical perspectives
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