Angels in disguise: sympatric hybridization in the marine angelfishes is widespread and occurs between deeply divergent lineages

Abstract

Hybridization events are not uncommon in marine environments where physical barriers are attenuated. Studies of coral reef taxa have suggested that hybridization predominantly occurs between parapatric species distributed along biogeographic suture zones. By contrast, little is known about the extent of sympatric hybridization on coral reefs, despite the large amount of biogeographic overlap shared by many coral reef species. Here, we investigate if the propensity for hybridization along suture zones represents a general phenomenon among coral reef fishes, by focusing on the marine angelfishes (family Pomacanthidae). Although hybridization has been reported for this family, it has not been thoroughly surveyed, with more recent hybridization studies focusing instead on closely related species from a population genetics perspective. We provide a comprehensive survey of hybridization among the Pomacanthidae, characterize the upper limits of genetic divergences between hybridizing species and investigate the occurrence of sympatric hybridization within this group. We report the occurrence of hybridization involving 42 species (48% of the family) from all but one genus of the Pomacanthidae. Our results indicate that the marine angelfishes are among the groups of coral reef fishes with the highest incidences of hybridization, not only between sympatric species, but also between deeply divergent lineages.

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

“…Parallel hybrid phenomena may occur in the angelfishes (Pomacanthidae). A recent survey of hybridization within the Pomacanthidae found that 59% of 37 hybridizing species pairs had sympatric distributions (defined by 50% range overlap) and some species pairs had older divergence dates as indicated by mtCO1 divergence between 5 and 8% [ 24 ]. Intriguingly, protogynous hermaphroditism is common in both the parrotfishes and the angelfishes, with mating system attributes that may facilitate heterospecific mating, as described under The breakdown of pre-mating isolation.…”

“…Intriguingly, protogynous hermaphroditism is common in both the parrotfishes and the angelfishes, with mating system attributes that may facilitate heterospecific mating, as described under The breakdown of pre-mating isolation. On the other hand, in 85% (n = 20) of angelfish hybrid zones where observations of abundance were available, one or both parental species were rare [ 24 ], an ecological pattern that clearly does not apply to the Scarus hybrid complex in the TEP where all three parental species are conspicuously abundant (Fig. 5 ).…”

“…Fishes living on coral reefs are offering an increasing number of examples of variation in the dynamics of hybridisation, with an accelerating number of studies documenting hybrid zones in a diversity of evolutionary clades and biogeographical contexts [ 17 – 24 ]. The relatively high number of cases of hybridization documented across several ecologically important and diverse families of reef fishes, particularly the butterflyfishes (Chaetodontidae), angelfishes (Pomacanthidae), and wrasses (Labridae) [ 25 ], provide exciting opportunities to apply a comparative approach to hybridization and introgression in the wild, with the potential to illuminate the ecological, behavioural, and developmental mechanisms that facilitate or limit hybridization [ 19 , 24 , 26 ].…”

Do phylogeny and habitat influence admixture among four North American chickadee (family: Paridae) species?

“…By comparison Randler (2006) found that hybridization was more frequent between parapatric than sympatric species, although Randler notes that there are exceptions to this pattern and similar to Willis et al (2014) states that sympatry may increase the potential for individuals to find mates (Tubaro and Lijtmaer 2002). Across taxa there is growing evidence that hybridization is common in natural populations among deeply divergent lineages and that sympatry may help to facilitate these events (Jasso-Martínez et al 2018, Tea et al 2020.…”

“…Hybridization is common in natural populations. Although it was previously thought that hybridization occurred exclusively between closely related species (Dasmahapatra et al 2007), it is now recognized that hybridization occurs between deeply divergent lineages (Jasso‐Martínez et al 2018, Joseph et al 2019, Tea et al 2020). Questions remain about the processes that facilitate the events; for example does hybridization occur because species live in sympatry or does hybridization occur because species exhibit ecological or habitat similarities (Willis et al 2014, Wood et al 2016, Kyogoku and Kokko 2019)?…”