Fish genital shape linked to predation

October 11, 2013

When predators lurk nearby, male Bahamas mosquitofish (Gambusia hubbsi) change mating strategies, rejecting elaborate courting rituals for more frequent and sometimes forceful encounters with females.

But as a recent North Carolina State University study shows, mating strategies aren't the only things changing for G. hubbsi when predators abound. The shape and size of the male fish's genitalia are also linked to the presence or absence of predators.

NC State Ph.D. student Justa Heinen-Kay and assistant professor of biological sciences R. Brian Langerhans show, in a paper published in the Journal of Evolutionary Biology, that fish coexisting with predators have longer, bonier and more elongated gonopodium tips than fish living without threat of predation. The gonopodium is the sperm-transferring organ in these livebearing fish.

Longer, bonier and more elongated gonopodium tips are, of course, relative; in small fish, these organ tips are generally only 1 millimeter long. Yet the findings suggest that male fish under constant threat of serving as a predator's snack have evolved better ways to impregnate females under these conditions.

"When predators are around, G. hubbsi males spend a lot of time attempting to mate with females because of the high mortality rate," Heinen-Kay said. "We hypothesize that G. hubbsi have evolved these bonier and more elongated gonopodium tips as a way to copulate even when females don't cooperate."

"Essentially, males need to transfer as much sperm as possible as quickly as possible, and this shape difference could help facilitate that," Langerhans said.

The researchers conducted the study in so-called "blue holes" in the Bahamas. These "big test tubes" are caves that have filled with water in the past 17,000 years; Langerhans calls them aquatic islands in a sea of land. Some of these aquatic islands contain Gambusia predators, while others do not.

"Comparing Gambusia across blue holes reveals that predation is associated with evolutionary changes in male genital shape," Langerhans said. "It's a beautiful and elegant system to study the causes and predictability of evolutionary changes."
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Note to editors: An abstract of the paper follows.

Predation-associated divergence of male genital morphology in a livebearing fish

Authors: Justa L. Heinen-Kay and Brian Langerhans, North Carolina State University
Published: October 2013, in Journal of Evolutionary Biology
DOI: 10.5061/dryad.g9735

Abstract: Male genital morphology is remarkably diverse across internally fertilizing animals, a phenomenon largely attributed to sexual selection. Ecological differences across environments can alter the context of sexual selection, yet little research has addressed how this may influence the rapid, divergent evolution of male genitalia. Using the model system of Bahamas mosquitofish (Gambusia hubbsi) undergoing ecological speciation across blue holes, we used geometric morphometric methods to test (i) whether male genital shape (the small, approximately 1 mm long, distal tip of the sperm-transfer organ, the gonopodium) has diverged between populations with and without predatory fish and (ii) whether any observed divergence has a genetic basis. We additionally examined the effects of genetic relatedness and employed model selection to investigate other environmental factors (i.e. interspecific competition, adult sex ratio and resource availability) that could potentially influence genital shape via changes in sexual selection. Predation regime comprised the most important factor associated with male genital divergence in this system, although sex ratio and some aspects of resource availability had suggestive effects. We found consistent, heritable differences in male genital morphology between predation regimes: Bahamas mosquitofish coexisting with predatory fish possessed more elongate genital tips with reduced soft tissue compared with counterparts inhabiting blue holes without predatory fish. We suggest this may reflect selection for greater efficiency of sperm transfer and fertilization during rapid and often forced copulations in high-predation populations or differences in sexual conflict between predation regimes. Our study highlights the potential importance of ecological variation, particularly predation risk, in indirectly generating genital diversity.

North Carolina State University

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