Life at low temperatures: A novel breeding-system adjustment in a polar cladoceran

The typical breeding system of cladocerans, cyclic parthenogenesis, is poorly suited to polar settings because it requires one or more rounds of parthenogenesis before the production of males and sexual eggs. Past work has shown that many arctic cladocerans have secondarily made the transition to obligate, apomictic parthenogenesis. Arctic populations of Holopedium gibberum lack males, suggesting their possible adoption of this breeding system. However, this study shows that these lineages instead possess genotypic characteristics expected under either selffertilization or automictic parthenogenesis, the first record of such a breeding system in the Cladocera. As populations of Holopedium from southerly areas reproduce by cyclic parthenogenesis, this breeding system transition appears to represent an adaptive response to living at low temperatures. The elevated incidence of asexual reproduction in populations that inhabit extreme environments—a pattern termed geographic parthenogenesis—has been widely recognized for both plant (e.g., Bierzychudek 1985) and animal groups (e.g., Glesener and Tilman 1978). The varied explanations for this pattern, which may often act synergistically, have included the demographic benefits of unisexuality in low-productivity environments, relaxation of biotic selection pressures for the maintenance of sex (Glesener and Tilman 1978), the advantages of polyploidy in cold conditions (Grime and Mowforth 1982; Stebbins 1984; Dufresne and Hebert 1998), and the benefits of genetic diversity linked to the role of hybridization in generating many asexuals (Kearney 2005). However, in some cases the breeding-system transition may have a simpler selective basis; it may be a necessary precondition for colonization of the extreme environment. The typical breeding system of cladocerans, cyclic parthenogenesis, aids both the founding of populations from single individuals and their rapid numerical increase where conditions allow multiple generations of parthenogenesis. However, in the north, this breeding system can lead to a fatal delay in the production of diapausing eggs and to the exclusion of species because slowed developmental rates at low temperatures prevent completion of a life cycle (Hebert and Hann 1986). In fact, the paucity of cladocerans in the arctic has been linked to this penalty of cyclic parthenogenesis (Hebert and Hann 1986). Interestingly, past studies have revealed that breeding-system adjustments are common in the few cladocerans that have colonized polar habitats. For example, the sole Bosmina species, as well as several species in the genus Daphnia, have abandoned sexual reproduction in arctic settings (Little et al. 1997; Weider et al. 1999). Obligate parthenogenesis is indeed far more prevalent among arctic Daphnia than among their temperate counterparts. Of the 34 species of Daphnia documented for North America (Hebert 1995), 30 of which occur in temperate regions, only two exhibit obligate parthenogenesis in southern locales (Černý and Hebert 1993; Hebert et al. 1993; Hebert and Finston 2001). On the other hand, of the 10 species with distributions that include habitats north of the Arctic Circle (see Hebert 1995), at least four species are known to reproduce parthenogenetically there (see Weider et al. 1999). In the particularly harsh eastern North American arctic, at least 3 of the 5 species that occur there are obligates. In fact, among the Cladocera, just one definitively known cyclical parthenogen is known from the high arctic of North America—Chydorus sphaericus, a diminutive species with rapid development times (Boileau et al. 1992). Several species of confirmed cyclical parthenogens have been studied in northern Europe at around 60uN latitude (e.g., Ebert et al. 2002; Haag et al. 2002, 2006), but genetic diagnoses in other areas are necessary because climatic conditions in Europe are generally milder than at North American sites of similar latitude. The present study extends investigations to a new taxon, Holopedium gibberum Zaddach 1855, which is dominant in many arctic lakes. H. gibberum s.l. occurs widely in the Northern Hemisphere, typically in lakes with low solute concentrations (Rowe 2000). It has been established that populations in the temperate regions of North America reproduce by cyclic parthenogenesis (Hebert and Finston 1997), but genetic diagnoses of breeding systems have not been carried out in other areas. However, ecological studies have revealed that populations in European lakes are reestablished each spring from resting eggs produced in the fall (Hrbáček pers. comm.). This observation implies that polar populations of Holopedium confront a serious challenge— they must complete their life cycle each year despite slowed 1 Corresponding author ([email protected]; phone: 1-519824-4120, ext. 56668; fax: 1-519-767-1656). Acknowledgments We thank Anders Hobæk, Martin Černý, and Miroslaw Slusarczyk for the European specimens of Holopedium, and Ian Smith for assistance with figures. Teri Crease, Jonathan Witt, and two anonymous reviewers provided helpful comments on the manuscript. This research was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) grant to P.D.N.H., by Ontario Graduate and NSERC scholarships to C.L.R., and by a NSERC postdoctoral fellowship to S.J.A. Limnol. Oceanogr., 52(6), 2007, 2507–2518 E 2007, by the American Society of Limnology and Oceanography, Inc.