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REVIEW Physiological Dependence on Copulation in Parthenogenetic Females Can Reduce the Cost of Sex

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REVIEW Physiological Dependence on Copulation in Parthenogenetic Females Can Reduce the Cost of Sex ANIMAL BEHAVIOUR, 2004, 67, 811e822 doi:10.1016/j.anbehav.2003.05.014 REVIEW Physiological dependence on copulation in parthenogenetic females can reduce the cost of sex M. NEIMAN Department of Biology, Indiana University, Bloomington (Received 6 December 2002; initial acceptance 10 April 2003; final acceptance 27 May 2003; MS. number: ARV-25) Despite the two-fold reproductive advantage of asexual over sexual reproduction, the majority of eukaryotic species are sexual. Why sex is so widespread is still unknown and remains one of the most important unanswered questions in evolutionary biology. Although there are several hypothesized mechanisms for the maintenance of sex, all require assumptions that may limit their applicability. I suggest that the maintenance of sex may be aided by the detrimental retention of ancestral traits related to sexual reproduction in the asexual descendants of sexual taxa. This reasoning is based on the fact that successful reproduction in many obligately sexual species is dependent upon the behavioural, physical and physiological cues that accompany sperm delivery. More specifically, I suggest that although parthenogenetic (asexual) females have no need for sperm per se, parthenogens descended from sexual ancestors may not be able to reach their full reproductive potential in the absence of the various stimuli provided by copulatory behaviour. This mechanism is novel in assuming no intrinsic advantage to producing genetically variable offspring; rather, sex is maintained simply through phylogenetic constraint. I review and synthesize relevant literature and data showing that access to males and copulation increases reproductive output in both sexual and parthenogenetic females. These findings suggest that the current predominance of sexual reproduction, despite its well-documented drawbacks, could in part be due to the retention of physiological dependence on copulatory stimuli in parthenogenetic females. Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Parthenogenetic reproduction has several selective advan- quickly outnumber the descendants of their sexual tages over sexual reproduction that should result in the progenitors. Based on this reasoning, populations com- elimination of sexuality (Maynard Smith 1978). The most prised of coexisting sexual and parthenogenetic forms relevant difference between sexual and parthenogenetic should be so evolutionarily transient that they are rarely, if reproduction is that parthenogenetic organisms do not ever, seen (Maynard Smith 1978). produce male offspring. This means that if two female Another important advantage of parthenogenesis is organisms are identical in every respect except that one directly related to differences in the mechanism that female reproduces parthenogenetically and the other parthenogens and sexuals use to transmit their genome produces offspring via sex, the parthenogen will produce from generation to generation. Because parthenogenetic two female offspring for every one female and one male organisms do not utilize genetic recombination to pro- offspring produced by the sexual female. Because only duce gametes, their offspring contain genomes that are, females can contribute directly to the rate of population barring mutation, wholly identical to that of their mother. growth, this simple difference between sexual and The genetic fidelity of parthenogenetic reproduction parthenogenetic reproduction means that the intrinsic relative to the recombinational mixing that accompanies rate of increase in a parthenogenetic population will be sex may constitute an evolutionary advantage if the par- exponentially higher than that of an equivalent sexual thenogens are optimally adapted to stable environmental population. Consequently, the descendants of a partheno- conditions (Williams 1975; Maynard Smith 1978). genetic mutant in a population of sexual organisms will These inescapable benefits of parthenogenetic reproduc- tion lead to the conclusion that parthenogenesis should Correspondence: M. Neiman, Department of Biology, Indiana Univer- be the rule rather than the exception. However, biological sity, 1001 E. 3rd Street, Bloomington, IN 47405, U.S.A. (email: reality clearly shows that sex dominates the vast majority [email protected]). of natural populations (Maynard Smith 1978). This 811 0003e3472/03/$30.00/0 Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. 812 ANIMAL BEHAVIOUR, 67, 5 discrepancy between theoretical prediction and biological Selection will tend to favour organisms that couple reality remains largely unexplained (reviewed in West costly resource investment with appropriate and reliable et al. 1999; Burt 2000). stimuli (Gill & Rissman 1997; Cheng et al. 1998; Ball & A variety of mechanisms such as mutation accumula- Bentley 2000; Lee & Gorman 2000; Schiml et al. 2000; tion and parasite pressure have been put forth as potential Wallen 2000; Wingfield et al. 2000). By definition, sexually explanations for the maintenance of sex (reviewed in West reproducing females need sperm to produce offspring. et al. 1999). Although several of these mechanisms, Sperm delivery in internally fertilized animals is almost including Muller’s ratchet (Muller 1964), the Red Queen invariably accompanied by courtship and/or copulation. (Hamilton 1980), and the mutational deterministic hy- The inevitable coupling of sperm delivery with stimuli pothesis (Kondrashov 1988) hold up well theoretically related to courtship and copulation, in conjunction with and have received some empirical support (e.g. Lively an extensive body of empirical support, has led to the 1987; Chao 1990; Dybdahl & Lively 1995, 1998), the strict conclusion that sexual behaviour above and beyond assumptions that must hold for any of these hypotheses sperm delivery per se is often a necessary prerequisite to limit their general application and prevent overall con- maximize reproductive output; that is, it acts as a primer sensus on the nature of the mechanism(s) behind the to stimulate and coordinate reproductive function in maintenance of sex (West et al. 1999). Also, several of internally fertilized sexual taxa (Moore et al. 1985a; these genetic mechanisms, most notably Muller’s ratchet, Schiml et al. 2000; Wallen 2000). operate too slowly to keep sexual lineages from being Molecular and biogeographical evidence indicates that outcompeted (Howard & Lively 1994). Thus, the identi- the vast majority of parthenogenetic species are recently fication of a mechanism that acts to reduce partheno- (!100 000 years) descended from sexual ancestors (e.g. genetic fitness immediately following a transition to Densmore et al. 1989; Sandoval et al. 1998). Williams (1975, asexuality is potentially valuable when considering the page 104) alluded to the possibility that recent descent of evolutionary forces that lead to the maintenance of sex asexuals from sexual ancestors may result in the retention (Simon et al. 2002). of dependence on stimuli related to fertilization in asexual A fundamental assumption of the demographic advan- females in a manner that could constrain the evolutionary tage of parthenogenetic reproduction is that a switch to potential of an asexual strategy. Analogously, it seems parthenogenesis does not result in decreased reproductive reasonable to suggest that many parthenogenetic species output (Lamb & Willey 1979). Key insights into the main- are likely to remain at least partially dependent on the tenance of sex can thus come from the elucidation of physiological response elicited by the stimuli of copulation. circumstances under which parthenogenetic reproduction The earlier stated assumption that a transition to is accompanied by reduced reproductive output. The pur- parthenogenetic reproduction does not decrease repro- pose of this review is to identify and provide support for ductive output may be violated if parthenogenetic females a nongenetic, constraint-based mechanism (i.e. partheno- (1) retain physiological dependence on copulatory stimuli genetic dependence on copulatory stimuli) by which the and (2) do not receive the amount of copulatory stimula- reproductive output of recently derived parthenogenetic tion required to realize the full two-fold advantage of females might be reduced relative to the reproductive producing all-female offspring. Under these circumstan- output of closely related sexual females. This mechanism ces, parthenogenetic females will not produce as many can provide a short-term advantage to sexual reproduction daughters as they would if they received the copulatory and could thus facilitate the maintenance of sex in a stimulation needed for optimal physiological priming. mixed population following the recent invasion of an The discrepancy between the number of offspring that asexual competitor. parthenogenetic females can produce and the number of offspring that they actually produce because they do not receive enough copulatory stimulation to reach their full PHYSIOLOGICAL DEPENDENCE ON reproductive potential could partially or even wholly COPULATION AS A MECHANISM FOR compensate for the two-fold cost of sex, particularly when THE MAINTENANCE OF SEX considered in combination with other theorized advan- tages of sex (e.g. West et al. 1999). I review theoretical and Consider a population of sexual organisms. Like the vast empirical evidence for the fulfilment of these conditions majority of eukaryotic taxa, their ancestors
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