Postcopulatory sexual selection generates speciation phenotypes in Drosophila.
BACKGROUND
Identifying traits that reproductively isolate species, and the selective forces underlying their divergence, is a central goal of evolutionary biology and speciation research. There is growing recognition that postcopulatory sexual selection, which can drive rapid diversification of interacting ejaculate and female reproductive tract traits that mediate sperm competition, may be an engine of speciation. Conspecific sperm precedence (CSP) is a taxonomically widespread form of reproductive isolation, but the selective causes and divergent traits responsible for CSP are poorly understood.


RESULTS
To test the hypothesis that postcopulatory sexual selection can generate reproductive isolation, we expressed GFP or RFP in sperm heads of recently diverged sister species, Drosophila simulans and D. mauritiana, to enable detailed resolution of species-specific sperm precedence mechanisms. Between-species divergence in sperm competition traits and mechanisms prompted six a priori predictions regarding mechanisms of CSP and degree of cross asymmetry in reproductive isolation. We resolved four distinct mechanisms of CSP that were highly consistent with predictions. These comprise interactions between multiple sex-specific traits, including two independent mechanisms by which females exert sophisticated control over sperm fate to favor the conspecific male.


CONCLUSIONS
Our results confirm that reproductive isolation can quickly arise from diversifying (allopatric) postcopulatory sexual selection. This experimental approach to "speciation phenotypes" illustrates how knowledge of sperm precedence mechanisms can be used to predict the mechanisms and extent of reproductive isolation between populations and species.
Department of Biology, Syracuse University, Syracuse, NY 13244, USA.
Mollie K
MK
Manier
Stefan
S
Lüpold
John M
JM
Belote
William T
WT
Starmer
Kirstin S
KS
Berben
Outi
O
Ala-Honkola
William F
WF
Collins
Scott
S
Pitnick
D000818:Animals; D003307:Copulation; D004330:Drosophila / Q000033:anatomy & histology* / Q000145:classification / Q000235:genetics*; D005260:Female; D005306:Fertilization / Q000502:physiology; D049810:Genetic Speciation; D049452:Green Fluorescent Proteins / Q000096:biosynthesis; D007314:Insemination / Q000502:physiology; D008164:Luminescent Proteins / Q000096:biosynthesis; D008297:Male; D060047:Reproductive Isolation; D012726:Sexual Behavior, Animal; D013045:Species Specificity; D013077:Sperm Head / Q000378:metabolism; D013094:Spermatozoa / Q000502:physiology; D000097573:Red Fluorescent Protein
D049452:Green Fluorescent Proteins; D008164:Luminescent Proteins; D000097573:Red Fluorescent Protein