The road that connects also divides.

This dichotomy – half-century-old roads connecting portions of Bahamian islands while fragmenting the tidal waters below – leads to rapid and interesting changes in the fish living in those fragmented sections, according to a new study from North Carolina State University.

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 Evolutionary Applications, that the male genitalia of three different species of Bahamian mosquitofish (Gambusia) living in fragmented waters differ markedly from the genitalia of fish living in unfragmented waters.

Fragmentation limits the number of mosquitofish predators, which appears to have a link to the shape of the male fish’s genitalia. Fish coexisting with predators in unfragmented areas have bonier and more elongated gonopodium tips than fish living without threat of predation in fragmented areas. The gonopodium is the sperm-transferring organ in these livebearing fish.

“This study shows that human-induced habitat alteration results in changes in fish genitalia in just 35 to 50 years – the time elapsed since the fragment-causing roads were built,” Heinen-Kay said. “While we expected to see some changes, we were surprised to see the consistency with which each species changed in accordance with our predictions based on earlier work that focused on how ecological factors, such as predation, affected the evolution of male genitalia over the course of thousands of years.”

The authors said that these findings indicate that sometimes the impacts of human activities on the traits of organisms can be predictable, suggesting that management, restoration and conservation efforts could be useful.

Langerhans added that the study could provide particular insight into speciation, or how different species develop.

“Because genitalia have an obvious and direct influence on reproduction, these findings beg the question of whether human-induced environmental change might facilitate speciation. As populations become more and more different in their genital morphology, their ability to interbreed can decline, leading to speciation,” Langerhans said. “How common this sort of rapid change in genital shape might be in other species, and its consequences for the formation of new species, are some of the questions we’ll ask in future studies.”

Dr. Craig Layman, an NC State associate professor of applied ecology, and Holly Noel, an undergraduate student in biological sciences at NC State, co-authored the paper. The research was supported by the National Science Foundation and NC State.

– kulikowski –

Note to editors: An abstract of the paper follows.

Human-caused habitat fragmentation can drive rapid divergence of male genitalia

Authors: Justa L. Heinen-Kay, Holly G. Noel, Craig A. Layman and Brian Langerhans, North Carolina State University

Published: November 2013 in Evolutionary Applications

DOI: 10.1111/eva.12223

Abstract: The aim of this study rests on three premises: (i) Humans are altering ecosystems worldwide, (ii) environmental variation often influences the strength and nature of sexual selection, and (iii) sexual selection is largely responsible for rapid and divergent evolution of male genitalia. While each of these assertions has strong empirical support, no study has yet investigated their logical conclusion that human impacts on the environment might commonly drive rapid diversification of male genital morphology. We tested whether anthropogenic habitat fragmentation has resulted in rapid changes in the size, allometry, shape, and meristics of male genitalia in three native species of livebearing fishes (genus: Gambusia) inhabiting tidal creeks across six Bahamian islands. We found that genital shape and allometry consistently and repeatedly diverged in fragmented systems across all species and islands. Using a model selection framework, we identified three ecological consequences of fragmentation that apparently underlie observed morphological patterns: decreased predatory fish density, increased conspecific density, and reduced salinity. Our results demonstrate that human modifications to the environment can drive rapid and predictable divergence in male genitalia. Given the ubiquity of anthropogenic impacts on the environment, future research should evaluate the generality of our findings and potential consequences for reproductive isolation.