Academic journal article Genetics

Cost of Interacting with Sexual Partners in a Facultative Sexual Microbe

Academic journal article Genetics

Cost of Interacting with Sexual Partners in a Facultative Sexual Microbe

Article excerpt

ABSTRACT

The widespread occurrence of sexual organisms despite the high costs of sex has long intrigued biologists. The best-known costs are the twofold cost of producing males and the cost associated with producing traits to attract mates and to interact with mating partners, such as exaggerated sexual behaviors and morphological modifications. These costs have been inferred from studies of plants and animals but are thought to be absent in facultative sexual microbes. Here, using the facultative sexual fungus Cryptococcus neoformans, I provide experimental evidence showing that: (i) interactions with active sexual partners can be costly for vegetative fitness in a facultative sexual microbe; (ii) this cost is positively correlated to mating ability; (iii) this cost is composed of at least two distinct components, the cost of producing mating signals that exert effects on mating partners and that associated with responding to active mating partners; and (iv) extended asexual reproduction can reduce both components of the cost. This cost must have been compensated for by the production of zygotes and sexual spores to allow the initial evolution and spread of sexual reproduction in eukaryotes.

SEX and sexual reproduction are widespread among eukaryotes (BELL 1982). Mating-the fusion of genetically differentiated gametes-is an essential feature of all sexual reproductive cycles. Evolutionary studies indicate that eukaryotic sexual reproduction has an ancient origin: it likely evolved among the first eukaryotic microbes (MiCHOD and LEVIN 1988; BACKS and ROGER 1999). The ubiquitous distribution of sex and sexual reproduction among all eukaryotic phyla suggests an essential role of sexual reproduction in the diversification and evolution of eukaryotes. However, theoretical and empirical investigations of sexually dimorphic eukaryotes such as insects, birds, and mammals suggest that sex and sexual reproduction can be costly (MICHOD and LEVIN 1988), the most discussed being the twofold cost of producing males and the cost associated with producing exaggerated sexual behaviors and morphological modifications (BELL and KOUFOPANOU 1986; MICHOD and LEVIN 1988). However, these costs are thought to be absent in facultative sexual microbes.

Unlike obligate sexual organisms such as the majority of higher plants and animals, sex and reproduction can be easily separated in facultative sexual microbes (Xu 2004a). One major component of sexual fitness in all sexual eukaryotes is mating success rate (BELL and KOUFOPANOU 1986; Xu 1995, 2002; Xu et al 1996). In many microbial eukaryotes, mating between compatible partners occurs only under certain stressful conditions. Under these conditions, both mating (i.e., the formation of zygotes) and vegetative growth of individual mating partners may occur. Using appropriately marked strains, all three cell types (i.e., the two parental types and the zygotes) in such a mating mixture can be directly counted using selective media. From these cell counts, the mating success rate and the relative vegetative fitness of the parental strains can be estimated. The vegetative fitness of individual parental strains in the presence of an active mating partner may change in comparison to that in the absence of such a partner. If the vegetative fitness were lower in the presence of an active mating partner, the reduction would constitute one type of cost of sex, i.e., the cost of interacting with a mating partner. Surprisingly, such a cost has never been evaluated or documented for any facultative sexual organisms.

Here, I used genetically marked strains of the facultative sexual fungus Cryptococcus neoformans to examine whether such a cost exists. C. neoformans is an encapsulated basidiomycetous yeast (CASADEVALL and PERFECT 1998) and is an emerging model organism for studying fungal molecular and evolutionary biology (e.g., LENGELER et al. 2000; HULL and HEITMAN 2002; Xu 2002, 2004b; Xu and MITCHELL 2003). …

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