Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation

• Published in: Molecular Biology and Evolution
• Main Authors: Masello, Juan, Quillfeldt, Petra, Sandoval-Castellanos, Edson, Alderman, Rachael, Calderón, Luciano, Cherel, Yves, Cole, Theresa, Cuthbert, Richard, Marin, Manuel, Massaro, Melanie, Navarro, Joan, Phillips, Richard, A., Ryan, Peter, Y. A., Shepherd, Lara, Suazo, Cristián, Weimerskirch, Henri, Moodley, Yoshan
• Other Authors: Department of Animal Ecology & Systematics Germany, Justus-Liebig-Universität Gießen = Justus Liebig University (JLU), Department of Animal Ecology and Systematics, Institute of Animal Breeding and Husbandry, Christian-Albrechts-Universität zu Kiel = Christian-Albrechts University of Kiel = Université Christian-Albrechts de Kiel (CAU), Department of Primary Industries Australia, Department of Primary Industries, Parks, Water and Environment, Centre d'Études Biologiques de Chizé - UMR 7372 (CEBC), Institut National de la Recherche Agronomique (INRA)-La Rochelle Université (ULR)-Centre National de la Recherche Scientifique (CNRS), RSPB Centre for Conservation Science, Royal Society for the Protection of Birds (RSPB), Section of Ornithology, Natural History Museum of Los Angeles County USA, Natural History Museum of Los Angeles County, Institute for Land, Water and Society, Charles Sturt University, Albury, NSW, Australia, Charles Sturt University Australia, Institute of Marine Sciences / Institut de Ciències del Mar Barcelona (ICM), Consejo Superior de Investigaciones Cientificas España = Spanish National Research Council Spain (CSIC), British Antarctic Survey (BAS), Natural Environment Research Council (NERC), FitzPatrick Institute of African Ornithology, University of Cape Town-DST-NRF Centre of Excellence, Museum of New Zealand - Te Papa Tongarewa, Justus Liebig University Giessen, Department of Zoology, University of Venda South Africa, University of Venda South Africa (UNIVEN)
• Format: Article in Journal/Newspaper
• Language: English
• Published: HAL CCSD 2019
• Subjects: homoploid hybrid speciation; additive traits; increased hybrid fitness; Procellariiformes; reproductive isolation; seabird; [SDE]Environmental Sciences; Antarctic; Antarc*; Antarctic prion; Pachyptila desolata
• Online Access: https://hal.science/hal-02199857; https://doi.org/10.1093/molbev/msz090

International audience Speciation through homoploid hybridization (HHS) is considered extremely rare in animals. This is mainly because the establishment of reproductive isolation as a product of hybridization is uncommon. Additionally, many traits are underpinned by polygeny and/or incomplete dominance, where the hybrid phenotype is an additive blend of parental characteristics. Phenotypically intermediate hybrids are usually at a fitness disadvantage compared with parental species and tend to vanish through backcrossing with parental population(s). It is therefore unknown whether the additive nature of hybrid traits in itself could lead successfully to HHS. Using a multi-marker genetic data set and a meta-analysis of diet and morphology, we investigated a potential case of HHS in the prions (Pachyptila spp.), seabirds distinguished by their bills, prey choice, and timing of breeding. Using approximate Bayesian computation, we show that the medium-billed Salvin’s prion (Pachyptila salvini) could be a hybrid between the narrow-billed Antarctic prion (Pachyptila desolata) and broad-billed prion (Pachyptila vittata). Remarkably, P. salvini’s intermediate bill width has given it a feeding advantage with respect to the other Pachyptila species, allowing it to consume a broader range of prey, potentially increasing its fitness. Available metadata showed that P. salvini is also intermediate in breeding phenology and, with no overlap in breeding times, it is effectively reproductively isolated from either parental species through allochrony. These results provide evidence for a case of HHS in nature, and show for the first time that additivity of divergent parental traits alone can lead directly to increased hybrid fitness and reproductive isolation.