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

Abstract

Background In 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. Results A 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. Conclusions Mating 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.

Assessing phenovariant species pairs of moray eels: Hybridization, introgression, and morphology

“…The hybridization between G. kidako and G. prionodon suggests interbreeding of morays does not necessarily occur in the most closely related species pair. A similar phenomenon was also observed in jacks ( Caranx , Carangidae), parrotfishes ( Scarus , Scaridae), and angelfishes (Pomacanthidae), in which the COI genetic divergence of a heterospecific pair can be up to 11.7% (Angulo et al, 2020; Carlon et al, 2021; Tea et al, 2020). Montanari et al (2014 and references therein) inferred from numerous studies on the Chaetodontidae and proposed that the incidence and extent of hybridization may be negatively related to the level of genetic divergence between the pair species.…”

“…DiBattista et al, 2015; Montanari et al, 2014). Hybrid offspring that possess intermediate colouration patterns of their parental species can result in taxonomic uncertainties, and in rare cases, non‐valid species, such as anemonefish Amphiprion leucokranos (Pomacentridae) and the parrotfish Scarus compressus (Scaridae) which have been subsequently demonstrated as hybrid populations (Carlon et al, 2021; Gainsford et al, 2015).…”

Hidden in the ocean: The importance of detecting hybridisation in pelagic and deep‐water fishes

“…On the contrary, when hybrids are fertile and viable, they can replace rare parental genotypes (genetic swamping), with a similar outcome of local extinction. With respect to phylogenetic distance between parental species, a recent study (Carlon et al, 2021) on the azure parrotfish (Scarus compressus, Scaridae) showed patterns consistent with a sharp decline in fitness in later-generation hybrids of species with older divergence, while this pattern was not observed in more recently diverged species. As hybridisation can be either a threat to species survival or a potential pathway to evolutionary rescue, it is unsurprising how the interest in hybridisation is gradually increasing in the more applied areas of conservation and resource management (Ottenburghs, 2020).…”

“…Indeed, Montanari et al (2016) suggested that, at the time of their study, 74% of marine fish hybrids had been reported since 1990, and further cases of hybridisation have been reported recently for example in eels (Anguilla spp., Anguillidae; Barth et al, 2020) and parrotfish (Carlon et al, 2021).…”

“…As mtDNA is uniparentally inherited, a measurable discrepancy between data types is also expected in hybrids whose quantitative phenotypes are perfectly intermediate but genetic data includes mitochondrial genes and when using small panels of well-characterised (diagnostic) nuclear and mitochondrial genetic markers (e.g. Carlon et al, 2021). Clearly, different data types may be inconsistent due to other factors.…”