Does genetic distance between parental species influence outcomes of hybridization among coral reef butterflyfishes?

Christmas Island is located at the overlap of the Indian and Pacific Ocean marine provinces and is a hot spot for marine hybridization. Here, we evaluate the ecological framework and genetic consequences of hybridization between butterflyfishes Chaetodon guttatissimus and Chaetodon punctatofasciatus. Further, we compare our current findings to those from a previous study of hybridization between Chaetodon trifasciatus and Chaetodon lunulatus. For both species groups, habitat and dietary overlap between parental species facilitate frequent heterospecific encounters. Low abundance of potential mates promotes heterospecific pair formation and the breakdown of assortative mating. Despite similarities in ecological frameworks, the population genetic signatures of hybridization differ between the species groups. Mitochondrial and nuclear data from C. guttatissimus × C. punctatofasciatus (1% divergence at cyt b) show bidirectional maternal contributions and relatively high levels of introgression, both inside and outside the Christmas Island hybrid zone. In contrast, C. trifasciatus × C. lunulatus (5% cyt b divergence) exhibit unidirectional mitochondrial inheritance and almost no introgression. Back-crossing of hybrid C. guttatissimus × C. punctatofasciatus and parental genotypes may eventually confound species-specific signals within the hybrid zone. In contrast, hybrids of C. trifasciatus and C. lunulatus may coexist with and remain genetically distinct from the parents. Our results, and comparisons with hybridization studies in other reef fish families, indicate that genetic distance between hybridizing species may be a factor influencing outcomes of hybridization in reef fish, which is consistent with predictions from terrestrially derived hybridization theory.

Naturally occurring hybrids of coral reef butterflyfishes have similar fitness compared to parental species.

Hybridisation can produce evolutionary novelty by increasing fitness and adaptive capacity. Heterosis, or hybrid vigour, has been documented in many plant and animal taxa, and is a notable consequence of hybridisation that has been exploited for decades in agriculture and aquaculture. On the contrary, loss of fitness in naturally occurring hybrid taxa has been observed in many cases. This can have negative consequences for the parental species involved (wasted reproductive effort), and has raised concerns for species conservation. This study evaluates the relative fitness of previously documented butterflyfish hybrids of the genus Chaetodon from the Indo-Pacific suture zone at Christmas Island. Histological examination confirmed the reproductive viability of Chaetodon hybrids. Examination of liver lipid content showed that hybrid body condition was not significantly different from parent species body condition. Lastly, size at age data revealed no difference in growth rates and asymptotic length between hybrids and parent species. Based on the traits measured in this study, naturally occurring hybrids of Chaetodon butterflyfishes have similar fitness to their parental species, and are unlikely to supplant parental species under current environmental conditions at the suture zone. However, given sufficient fitness and ongoing genetic exchange between the respective parental species, hybrids are likely to persist within the suture zone.

Reef fish hybridization: lessons learnt from butterflyfishes (genus Chaetodon).

Natural hybridization is widespread among coral reef fishes. However, the ecological promoters and evolutionary consequences of reef fish hybridization have not been thoroughly evaluated. Butterflyfishes form a high number of hybrids and represent an appropriate group to investigate hybridization in reef fishes. This study provides a rare test of terrestrially derived hybridization theory in the marine environment by examining hybridization between Chaetodon trifasciatus and C. lunulatus at Christmas Island. Overlapping spatial and dietary ecologies enable heterospecific encounters. Nonassortative mating and local rarity of both parent species appear to permit heterospecific breeding pair formation. Microsatellite loci and mtDNA confirmed the status of hybrids, which displayed the lowest genetic diversity in the sample and used a reduced suite of resources, suggesting decreased adaptability. Maternal contribution to hybridization was unidirectional, and no introgression was detected, suggesting limited, localized evolutionary consequences of hybridization.Comparisons to other reef fish hybridization studies revealed that different evolutionary consequences emerge, despite being promoted by similar factors, possibly due to the magnitude of genetic distance between hybridizing species. This study highlights the need for further enquiry aimed at evaluating the importance and long-term consequences of reef fish hybridization.