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Why stream mayflies can reproduce without males but remain bisexual: a case of lost genetic variation

350 210 Stroud Water Research Center

Funk, D.H., B.W. Sweeney, and J.K. Jackson. 2010. Journal of the North American Benthological Society 29:1258–1266.

doi:10.1899/10-015.1

Abstract

Mayflies (Ephemeroptera) are important to the food web of most stream, river, and lake ecosystems and are critical to water-quality monitoring programs. They are widespread and ancient (predate dinosaurs) and have primitive reproductive systems and the shortest adult life spans of all insects. Here we formulate and test the hypothesis that facultative parthenogenesis occurs as a widespread adaptation in most, if not all, mayflies. A rare form of reproduction, facultative parthenogenesis combines the short-term advantages of parthenogenesis, which doubles reproductive output, with the long-term advantages of genetic variation associated with sex. For 7 species of bisexual mayflies, we show that their eggs hatched whether fertilized or not and that unfertilized eggs took longer to develop and hatch. However, once hatched, larvae produced via parthenogenesis grew and developed to the adult in a manner similar to that of larvae produced sexually. In addition, for all study species, female adults produced parthenogenetically were diploid and could reproduce either sexually (producing males and females equally) or parthenogenetically (producing mostly females and some males). Males produced parthenogenetically were viable and occurred either as 1st generation (F1) offspring or as offspring of F1 gynandromorphs (intersex individuals). Last, we show that parthenogenetic descendants lose ~10 to 22% of their genetic variation as a result of each parthenogenetic generation. We use these findings and observations and other published data to support the hypothesis that most, if not all, mayflies are facultatively parthenogenetic. We propose that this ability increases mayfly reproductive success by giving eggs from unmated or incompletely fertilized females a 2nd chance. We then formulate 3 additional hypotheses: 1) parthenogenetic development of mayfly eggs proceeds automatically soon after emergence but can be and normally is preempted by fertilization, and that this mechanism both helps to compensate for and is enabled by the peculiarities of life history and primitive reproductive biology in this ancient group; 2) that facultative parthenogenesis enhances mayfly dispersal and gene flow because it enables virgin females to transfer genes within and among catchments and to form bisexual populations in new habitat; and 3) that mayflies remain bisexual despite being able to reproduce without males because of lost genetic variation associated with the parthenogenetic process.

Funding

NSF Award No. DEB-1052716 Title: LTREB: Trajectory for the recovery of stream ecosystem structure and function during reforestation. Principal Investigator: L. A. Kaplan. Co-principal investigators: A.K. Aufdenkampe, W.H. Eldridge, J.K. Jackson and J. Kan.