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

Juan F. Masello, Petra Quillfeldt, Edson Sandoval-Castellanos, Rachael Alderman, Luciano Calderón, Yves Cherel, Theresa L. Cole, Richard J. Cuthbert, Manuel Marin, Melanie Massaro, Joan Navarro, Richard A. Phillips, Peter G. Ryan, Lara D. Shepherd, Cristián G. Suazo, Henri Weimerskirch, Yoshan Moodley, Claudia Russo (Editor)

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish
Pages (from-to)1671-1685
Number of pages15
JournalMolecular Biology and Evolution
Volume36
Issue number8
Early online date26 Apr 2019
DOIs
Publication statusPublished - 01 Aug 2019

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Reproductive Isolation
Prions
reproductive isolation
prions
Breeding
fitness
breeding
hybridization
Inbreeding
incomplete dominance
Genetic Markers
metadata
backcrossing
meta-analysis
Meta-Analysis
genetic marker
seabird
blended foods
seabirds
phenology

Cite this

Masello, J. F., Quillfeldt, P., Sandoval-Castellanos, E., Alderman, R., Calderón, L., Cherel, Y., ... Russo, C. (Ed.) (2019). Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation. Molecular Biology and Evolution, 36(8), 1671-1685. https://doi.org/10.1093/molbev/msz090
Masello, Juan F. ; Quillfeldt, Petra ; Sandoval-Castellanos, Edson ; Alderman, Rachael ; Calderón, Luciano ; Cherel, Yves ; Cole, Theresa L. ; Cuthbert, Richard J. ; Marin, Manuel ; Massaro, Melanie ; Navarro, Joan ; Phillips, Richard A. ; Ryan, Peter G. ; Shepherd, Lara D. ; Suazo, Cristián G. ; Weimerskirch, Henri ; Moodley, Yoshan ; Russo, Claudia (Editor). / Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation. In: Molecular Biology and Evolution. 2019 ; Vol. 36, No. 8. pp. 1671-1685.
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Masello, JF, Quillfeldt, P, Sandoval-Castellanos, E, Alderman, R, Calderón, L, Cherel, Y, Cole, TL, Cuthbert, RJ, Marin, M, Massaro, M, Navarro, J, Phillips, RA, Ryan, PG, Shepherd, LD, Suazo, CG, Weimerskirch, H, Moodley, Y & Russo, C (ed.) 2019, 'Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation', Molecular Biology and Evolution, vol. 36, no. 8, pp. 1671-1685. https://doi.org/10.1093/molbev/msz090

Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation. / Masello, Juan F.; Quillfeldt, Petra; Sandoval-Castellanos, Edson; Alderman, Rachael; Calderón, Luciano; Cherel, Yves; Cole, Theresa L.; Cuthbert, Richard J.; Marin, Manuel; Massaro, Melanie; Navarro, Joan; Phillips, Richard A.; Ryan, Peter G.; Shepherd, Lara D.; Suazo, Cristián G.; Weimerskirch, Henri; Moodley, Yoshan; Russo, Claudia (Editor).

In: Molecular Biology and Evolution, Vol. 36, No. 8, 01.08.2019, p. 1671-1685.

Research output: Contribution to journalArticle

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AU - Marin, Manuel

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Masello JF, Quillfeldt P, Sandoval-Castellanos E, Alderman R, Calderón L, Cherel Y et al. Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation. Molecular Biology and Evolution. 2019 Aug 1;36(8):1671-1685. https://doi.org/10.1093/molbev/msz090