Anisogamy, sexual selection, and the evolution and maintenance of sex

Abstract

SummaryIn the present paper we distinguish between two aspects of sexual reproduction. Genetic recombination is a universal feature of the sexual process. It is a primitive condition found in simple, single-celled organisms, as well as in higher plants and animals. Its function is primarily to repair genetic damage and eliminate deleterious mutations. Recombination also produces new variation, however, and this can provide the basis for adaptive evolutionary change in spatially and temporally variable environments.The other feature usually associated with sexual reproduction, differentiated male and female roles, is a derived condition, largely restricted to complex, diploid, multicellular organisms. The evolution of anisogamous gametes (small, mobile male gametes containing only genetic material, and large, relatively immobile female gametes containing both genetic material and resources for the developing offspring) not only established the fundamental basis for maleness and femaleness, it also led to an asymmetry between the sexes in the allocation of resources to mating and offspring. Whereas females allocate their resources primarily to offspring, the existence of many male gametes for each female one results in sexual selection on males to allocate their resources to traits that enhance success in competition for fertilizations. A consequence of this reproductive competition, higher variance in male than female reproductive success, results in more intense selection on males.The greater response of males to both stabilizing and directional selection constitutes an evolutionary advantage of males that partially compensates for the cost of producing them. The increased fitness contributed by sexual selection on males will complement the advantages of genetic recombination for DNA repair and elimination of deleterious mutations in any outcrossing breeding system in which males contribute only genetic material to their offspring. Higher plants and animals tend to maintain sexual reproduction in part because of the enhanced fitness of offspring resulting from sexual selection at the level of individual organisms, and in part because of the superiority of sexual populations in competition with asexual clones.

Nocturnal mating behaviour and dynamic male investment of copulation time in the southern blue-ringed octopus, Hapalochlaena maculosa (Cephalopoda: Octopodidae)

“…Males made more approaches than females, particularly when the availability of females was low, suggesting that males expend more effort than females to initiate copulation. This result is consistent with patterns observed across most animal groups where anisogamy exists (Kodric-Brown & Brown, 1987). Both males and females were approached in similar frequencies, and male-male mount attempts were very common, suggesting that H. maculosa could not discriminate the sex of approached conspecifics within trials.…”

“…Within these animal models, anisogamy, which is the differential investment between males and females towards their gametes, leads to the reproductive success of most females of these taxa to be limited by the resources they have access to, and male reproductive success to be primarily limited by the numbers of females they can successfully mate with (Kodric-Brown & Brown, 1987). Therefore, where anisogamy exists, sexual selection typically imposes females to selectively mate with higher quality and/or genetically compatible males, and males to evolve traits or behaviours that enable them to achieve more copulations with a higher number of females, and to attain greater fertilisation success with the females they mate with (Darwin, 1906;Bateson, 1983;Kodric-Brown & Brown, 1987).…”

Dietary stress does not strengthen selection against single deleterious mutations in Drosophila melanogaster

“…Selection on males in particular has been shown to be potentially important in the amelioration of mutation load because, in polygamous mating systems with low paternal investment, selection on males can reduce the frequency of deleterious alleles without causing a reduction in the mean fitness of the population (Manning, 1984;Kodric-Brown and Brown, 1987;Koeslag and Koeslag, 1993;Whitlock, 2000;Agrawal, 2001;Siller, 2001;Lorch et al, 2003). To date, the effect on male reproductive success has been quantified for 14 different mutations with significant deleterious effects on non-sexual fitness (Whitlock and Bourguet, 2000;Pischedda and Chippindale, 2005;Sharp and Agrawal, 2008).…”

Inbreeding reveals stronger net selection on Drosophila melanogaster males: implications for mutation load and the fitness of sexual females

“…At the same time, theory predicts that stronger sexual selection on males can lower the number of deleterious mutations affecting females at shared sexually selected loci (Agrawal, 2001;Siller, 2001). Taken together, these ideas imply that malebiased selection could be a force that improves mean female fitness on a genome-wide scale (Kodric-Brown and Brown, 1987;Whitlock and Agrawal, 2009). Under some conditions (for example, a diploid genomic mutation rate of 1 and selection on males being approximately twice as strong as selection on females), the mean fitness of females can be double that of females in asexual populations (Agrawal, 2001;Siller, 2001), potentially accounting for the cost of sexual reproduction.…”