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 language | English |
|---|---|
| Pages (from-to) | 1671-1685 |
| Number of pages | 15 |
| Journal | Molecular Biology and Evolution |
| Volume | 36 |
| Issue number | 8 |
| Early online date | 26 Apr 2019 |
| DOIs | |
| Publication status | Published - 01 Aug 2019 |
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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 journal › Article
TY - JOUR
T1 - Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation
AU - Masello, Juan F.
AU - Quillfeldt, Petra
AU - Sandoval-Castellanos, Edson
AU - Alderman, Rachael
AU - Calderón, Luciano
AU - Cherel, Yves
AU - Cole, Theresa L.
AU - Cuthbert, Richard J.
AU - Marin, Manuel
AU - Massaro, Melanie
AU - Navarro, Joan
AU - Phillips, Richard A.
AU - Ryan, Peter G.
AU - Shepherd, Lara D.
AU - Suazo, Cristián G.
AU - Weimerskirch, Henri
AU - Moodley, Yoshan
A2 - Russo, Claudia
PY - 2019/8/1
Y1 - 2019/8/1
N2 - 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.
AB - 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.
KW - Additive traits
KW - Homoploid hybrid speciation
KW - Increased hybrid fitness
KW - Procellariiformes
KW - Reproductive isolation
KW - Seabird
UR - http://www.scopus.com/inward/record.url?scp=85073466222&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85073466222&partnerID=8YFLogxK
U2 - 10.1093/molbev/msz090
DO - 10.1093/molbev/msz090
M3 - Article
C2 - 31028398
AN - SCOPUS:85073466222
VL - 36
SP - 1671
EP - 1685
JO - Molecular Biology and Evolution
JF - Molecular Biology and Evolution
SN - 0737-4038
IS - 8
ER -