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BEHAVIOUR, 2004, 67, 811e822 doi:10.1016/j.anbehav.2003.05.014

REVIEW Physiological dependence on in parthenogenetic can reduce the cost of

M. NEIMAN Department of , 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 , the majority of eukaryotic 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 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 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 ; 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, 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 do not ever, seen (Maynard Smith 1978). produce male offspring. This means that if two Another important advantage of 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 to pro- offspring produced by the sexual female. Because only duce , their offspring contain genomes that are, females can contribute directly to the rate of barring , 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 is almost including Muller’s ratchet (Muller 1964), the Red invariably accompanied by 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 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 had been below and in Table 1. sexual for countless generations. Much of the cellular machinery enabling the transition of asexuality to sex- Condition 1: Parthenogenetic Dependence uality, known as the ‘origin’ (rather than the ‘mainte- on Copulation nance’) of sexual reproduction, is likely to have evolved hundreds of millions of years ago in response to evolu- Evidence from sexual systems tionary forces that differ from those maintaining sex Some insight into whether parthenogenetic females today (Maynard Smith 1978, 1988; Crow 1988; Williams retain dependence on copulation comes from research 1988; Lenski 1999; West et al. 1999; Otto & Lenormand into the physiological effects of copulation in obligately 2002). The present-day predominance of sexual reproduc- sexual species. While copulation is obviously a reproduc- tion means that the relevant scale for understanding the tive requirement for these animals, many studies have evolutionary forces maintaining sex is that of an asexual found that copulation often continues even after adequate mutant invading a sexual population. sperm has been acquired and when no nutritional benefits Table 1. The reproductive output of a variety of sexual and parthenogenetic species, as well as reproductive output of these species with and without copulatory stimuli, whether their probability of copulation is frequency dependent, and whether there is spatial separation between sexual and parthenogenetic species

Frequency of copulation Frequency- Estimated relative to dependent Spatial segregation reproductive sexual probability between sexual and Mode of reproduction/taxon Species output XYfemale (%) of copulation asexual populations Source

Sexual lizard Cnemidophorus parvisocius 1.77* NA NA NA ? NA Walker 1981a, b Sexual lizard Cnemidophorus sacki 5.9* NA NA NA ? NA Walker 1981b Parthenogenetic lizard Cnemidophorus neomexicanus 2e3* 11 ? ? ? Cole & Townsend 1983 Parthenogenetic lizard Cnemidophorus sonorae 3.7* 1 1 ? ? Yes Cole & Townsend 1983; Routman & Hulse 1984 Parthenogenetic lizard Cnemidophorus uniparens 3e4* 0.5e1.0 0.75e1.5 ? ? No Crews 1975; Gustafson & Crews 1981; Monaco et al. 1983; Cuellar 1984; Crews et al. 1986; Crews & Moore 1993 Sexual fish Poecilia mexicana 46.8y NA NA NA ? NA Hubbs 1964 Pseudogamous fish Poecilia formosa 34.8y 0 0.75 10e33 Negative Yes Hubbs 1964; Balsano et al. 1981; Woodhead & Armstrong 1985; Ryan et al. 1996 Sexual Brachionus plicatilis ?NANANANANARuttner-Kolisko 1983; Go´mez & Serra 1996 Parthenogenetic rotifer Brachionus plicatilis ???83e100 No No Ruttner-Kolisko 1983; Go´mez & Serra 1996 Sexual fly Drosophila mercatorum 53.55* NA NA NA NA NA Carson et al. 1982; Crews et al. 1985 Parthenogenetic fly Drosophila mercatorum 55.9* 1115e90 ? No Carson et al. 1982; Crews et al. 1985 Sexual fish Poeciliopsis lucida 6e25y NA NA 100 Negative NA Schultz 1961, 1982; McKay 1971; Keegan-Rogers 1984 Pseudogamous fish Poeciliopsis spp. 2e7.7y 0 0.7e10e60 Negative No Schultz 1961, 1982; McKay 1971; Keegan-Rogers 1984 Sexual snail Potamopyrgus antipodarum 11.46y NA NA NA ? NA Jokela et al. 1997 Parthenogenetic snail Potamopyrgus antipodarum 10.12y 0.8 1.2 NA ? Yes Jokela et al. 1997 Sexual Ips acuminatus 42e50*z NA NA NA Positive NA Løyning & Kirkendall 1996; Løyning 2000 Pseudogamous beetle Ips acuminatus 24e47*z 0?0e100 Positive No Løyning & Kirkendall 1996; Løyning 2000 Sexual roach Pynoscelus indicus 39* NA NA NA ? NA Roth 1974 Parthenogenetic roach Pynoscelus surinamensis 15e34*z ?? ? ? NA Roth 1974 Sexual planthopper Muellerianella fairmairei 164e266*z NA NA NA ? NA Booij & Guldemond 1984 Pseudogamous planthopper Muellerianella fairmairei 217e296* ? 0.81e1.8 100 NA Yes Booij & Guldemond 1984 Sexual isopod provisorius 7yx NA NA NA NA NA Frankel 1978 Parthenogenetic isopod Trichoniscus pusillus pusillus 8yx ?? ? ? No Frankel 1978

X Z mean asexual reproductive output relative to sexual females when the asexual female does not copulate; Y Z mean asexual reproductive output relative to sexual females when the asexual female does copulate. X and Y were calculated only when parthenogenetic reproductive output was estimated under conditions where the parthenogens do and do not copulate. ? Z Cited sources did not provide the information required to calculate or determine the corresponding value. */clutch. yBrooded /female. zStrain dependent. REVIEW xFecundity is linked to size. Sexual females are smaller than parthenogens, but have higher reproductive output for their size. 813 814 ANIMAL BEHAVIOUR, 67, 5

(such as or nuptial gifts) are received in were housed with males whose copulatory organs had return (e.g. Wilson et al. 1965; Baur & Baur 1992; Arnqvist been experimentally removed. This effect persisted even & Nilsson 2000). when the intact males did not ejaculate, leading the Wilson et al. (1965) pioneered research directed at authors to suggest that the stimulatory effect was linked to determining whether the stimuli provided by copulation contact between the male copulatory organs and mecha- affect fecundity and . Their research indicated that noreceptors in the genital opening of the female rather levels of neurotransmitters, such as progesterone and than sperm delivery per se. oestrogen, that are important to creating and maintaining A recent review and meta-analysis of the effects of are positively correlated with copulatory fre- multiple in showed that production quency in rats. Similarly, Lanier et al. (1975) showed that increases with frequency of copulation even after ac- female golden hamsters are more likely to become preg- counting for the genetic and nutritional benefits of copu- nant when mated multiply rather than singly. lation (Arnqvist & Nilsson 2000; also see Ridley 1988; The most direct physiological connection established Walker et al. 1999). The authors concluded that the between copulatory frequency and reproduction is de- physiological stimuli provided by copulation, specifically, rived from research on cues that control mammalian the gonadotropic substances contained in male ejaculate ovulation, which has shown that ovulation in organisms that are known to stimulate female egg production such as , rabbits and mustelids will not occur without (reviewed in Eberhard & Cordero 1995), probably are the copulatory stimuli (e.g. Ramirez & Beyer 1988; Baum et al. main factors underlying the association between copula- 1990; reviewed in Schiml et al. 2000). More specifically, tion frequency and offspring production. these researchers showed that vaginal and cervical sti- Fertility and fecundity in several snail species are also mulation is required to release luteinizing , the linked to copulatory frequency. In general, copulation ac- hormone that controls mammalian ovulation. celerates the onset of and egg laying (Huignard These patterns are not confined to . A 1970 et al. 1977; van Duivenboden 1983), increases the study examining the initiation of oogenesis in cock- synthesis of important to egg production (van roaches determined that oocyte development in some Duivenboden 1983; Kunigelis & Saleuddin 1986; Bride cockroach species is repressed until copulation occurs et al. 1991; Saleuddin et al. 1991; Clelland et al. 2001) and (Roth 1970). Several years later, Lamb & Willey (1979) increases total egg production (Baur 1988; Baur & Baur were the first to suggest that the assumption that parthe- 1992). Research directed at determining the physiological nogens match the total reproductive output of their sexual mechanisms that underlie the connection between cop- progenitors is often violated. They supported this asserta- ulation and egg production in snails has also shown, as in tion by reviewing evidence that the fertility of partheno- insects, that substances transmitted by have genetic species is often low compared with that of a stimulatory effect on the production of hormones in closely related sexual species. Crews et al. (1985) showed the female that are important to reproduction (Huignard that the behavioural stimuli of copulation comprise an et al. 1977; Bride & Gomot 1991; Koene & Chase 1998). important positive factor affecting fecundity in sexual The wide variety of data suggesting that stimuli associ- Drosophila melanogaster. This result was corroborated by a ated with courtship and copulation interact with and sti- study of reproduction in the grasshopper Romalea micro- mulate physiological and behavioural processes to ensure ptera that detected a positive effect of copulation on the rate successful reproduction has led to general agreement that of egg development and oviposition (Walker et al. 1999). male courtship and mating behaviour are often important More direct insight into the question of the effects of facilitators of hormone secretion, ovarian development copulation on female reproduction is provided by studies and egg production in both and that control female access to males. Shahi & Krishna females (Crews 1975; Crews et al. 1985; Lindzey & Crews (1979) found that female moths (Earias fabia) that were 1986). allowed to see males produced more eggs than females that were housed alone, but not as many eggs as females Evidence for copulatory dependence in that were allowed full access to and multiple copulations parthenogenetic females with males. A similar, more recent study conducted by Surprisingly little work has been directed towards the Schmidt & Arbu¨tz (1994) showed that reproductive question of whether reproduction in parthenogens of activity was highest in female desert locusts, Schistocerca sexual ancestry is affected by copulation. Interestingly, gregaria, that were allowed full access to males, followed by despite the well-documented costs of copulation, such as females that were separated from males by a clear, porous time and energy expenditure, increased risk of , barrier, then by females that were housed alone. The and acquisition of parasites and pathogens, parthenogens authors presented these data as evidence for hormonal from a variety of taxa still copulate although they have no primers and behavioural releasers of male origin that are need of sperm (e.g. Roth 1967; Crews et al. 1986; Paulissen required by females to maximize reproductive output. An & Walker 1989; Go´mez & Serra 1996; unpublished data). It even more direct test of the connection between copula- seems reasonable to suggest that the retention of mating tory stimuli and reproduction was provided by Lefebvre & behaviour and the reliance on copulatory stimuli for Caudet (1999), who found that the onset of reproduction maximal reproductive output in a wide variety of was accelerated in female terrestrial (Armadil- parthenogenetic taxa derived from sexual ancestors could lidium vulgare) that were allowed to copulate with males be a direct result of the phylogenetic inertia that couples having intact copulatory organs relative to females that copulation with priming of reproductive physiology. REVIEW 815

This possibility is carried to a logical extreme in pseu- specifically, Crews & Moore (1986) and Crews et al. (1986) dogamous organisms (Maynard Smith 1986; Beukeboom found that the fecundity of females from two different & Vrijenhoek 1998), which produce eggs parthenogenet- parthenogenetic Cnemidophorus ‘species’ increased by ically but require the stimuli delivered by sperm entry into 30e60% following ‘copulation’ with a masculinized con- the egg to initiate division towards embryogenesis. In specific relative to the fecundity of lizards that did not general, it is thought that the sperm nucleus is sub- have access to . Other work has shown sequently ejected from the egg (e.g. Schlupp et al. 1994), that parthenogenetic Cnemidophorus are more likely to although the specific mechanism by which the genetic ovulate if housed with a male conspecific or a masculinized material of the male is excluded has not been established parthenogen than with an untreated female parthenogen for all identified pseudogamous species (Beukeboom & or alone (Gustafson & Crews 1981; Lindzey & Crews 1986). Vrijenhoek 1998). Regardless of the specific mechanism by These observations have led some Cnemidophorus re- which embryogenesis ensues, the resultant offspring are searchers to speculate that same-sex copulatory behaviour genetically identical to the mother (e.g. Schlupp et al. may have evolved in response to selection favouring 1994; reviewed in Beukeboom & Vrijenhoek 1998). While parthenogens that were able to solicit and participate in the evolutionary dynamics of coexisting sexual/pseudog- a ritual that incorporates key stimulatory elements of true amous populations are interesting in themselves (Stenseth copulation (Crews & Fitzgerald 1980; Moore et al. 1985a). et al. 1985; Kirkpatrick & Dugatkin 1994; Schartl et al. The striking ecological success of parthenogenetic Cnemi- 1995), the complete dependence of pseudogamous fe- dophorus, which often compete successfully with closely males on sperm provided by males of closely related related sexual species (e.g. Wright & Lowe 1968; Cuellar species results in inherent negative frequency-dependent 1979; Parker 1979), may be linked to their fortuitous and selection favouring sexual females whenever pseudoga- unique exploitation of behaviour that delivers the stimuli mous frequency is so high that males become limiting required for maximal reproduction. The simple existence (Moore & McKay 1971; Stenseth et al. 1985; Kirkendall of such a superficially superfluous behaviour may in fact 1990). This means that the maintenance of sex in mixed be a testament to the strength of the constraint posed by populations of sexual and pseudogamous individuals does asexual copulatory dependence. not constitute an evolutionary problem to the degree of While no research has directly addressed the effects of that presented by sexual coexistence with truly partheno- copulation on offspring production in parthenogenetic genetic organisms that can produce some offspring without , several invertebrate parthenogens do seem any input from males (Beukeboom & Vrijenhoek 1998). to have lower reproductive capacity than their sexual However, in an analogous sense to the ideas presented here, counterparts, a phenomenon that could be related to the advantage of producing all-female offspring decreases physiological dependence on copulation. For example, with decreased access of pseudogamous females to copula- Roth (1974) showed that the number of eggs produced tions (McKay 1971; Stenseth et al. 1985). and matured by parthenogenetic Suriname cockroaches, To date, the best-known examples of dependence of Pynoscelus surinamensis, was significantly less than the fecundity on copulation in sperm-independent partheno- number of eggs produced by their sexual progenitor gens come from the parthenogenetic lizards of the Cnemi- species P. indicus. The reason for the discrepancy in egg dophorus genus. Laboratory-based behavioural studies of production between the two types of roaches was not some of these species have shown that the parthenogens established, but Roth suggested that physiological stimu- actively solicit and engage in a wholly unique form of lation from sperm-filled spermathecae may be an impor- pseudocopulatory behaviour with fellow female parthe- tant determinant of successful offspring production. In nogens (Crews & Fitzgerald 1980; Moore et al. 1985b; addition, Frankel (1978) compared production in Crews 1989; Paulissen & Walker 1989). There is both sexual and parthenogenetic isopods (Trichoniscus spp.), indirect (Crews & Young 1991) and direct (Walker et al. and found that sexual females consistently carried quali- 1991) evidence suggesting that copulatory and pseudo- tatively more embryos for their size than parthenogenetic copulatory behaviour may be a common occurrence in females. In fact, he eventually used these productivity natural populations of parthenogenetic Cnemidophorus. differences to discriminate sexual from parthenogenetic Interestingly, pseudocopulatory behaviour has never been individuals. reported in sexual Cnemidophorus species (Crews & Fitzgerald 1980; Cole & Townsend 1983), or for that matter, in any other parthenogenetic taxon, suggesting Condition 2: Limited Access of Parthenogens that the of this behaviour in Cnemidophorus to Copulation may constitute a fortuitous evolutionary response to re- cent and novel selective pressures related to decreased ac- Male discrimination against parthenogenetic females cess to males following the transition to parthenogenesis. The ability to discriminate between potential mates of Research focused on detailing the physiological con- different phenotypes or even different genotypes may be sequences of pseudocopulation has shown that parthe- adaptive if the choice of the ‘wrong’ mate carries a net cost nogens that participate in pseudocopulatory behaviour for one or both individuals involved. This situation may are always reproductively active (Crews & Fitzgerald 1980; arise in cases where the pool of potential mates includes, Moore et al. 1985b). Importantly, this research has also for example, heterospecific individuals, parthenogenetic shown that there is a positive effect of pseudocopula- individuals or sterile individuals (e.g. McKay 1971; tory behaviour on the fecundity of parthenogens. More Kawecki 1988; Koeslag & Koeslag 1994; Erlandsson & 816 ANIMAL BEHAVIOUR, 67, 5

Kostylev 1995). Under these circumstances, the usual costs Frequency dependence of male mate selection of copulation, such as energy (e.g. Slagvold et al. 1988), Both theoretical and empirical work suggest that male time (Daly 1978), gametes (Dewsbury 1982; Nakatsuru & choosiness may be frequency dependent (e.g. McKay Kramer 1982; Sva¨rd & Wiklund 1986; Kirkendall 1990), 1971; Stenseth et al. 1985; Løyning & Kirkendall 1996; accessory secretion expenditure (Dewsbury 1982; Olsson Table 1). Real (1990) argued that, from the perspective of et al. 1997; Buckland-Nicks 1998), increased exposure to the choosing sex, as the variance in mate quality increases depredation (reviewed in Magnhagen 1991) and infec- and, critically, the mean of mate quality decreases (as it tion (Daly 1978; Westneat & Rambo 2000), are com- would if a population were increasingly comprised of pounded by the possibility that the copulation will not parthenogens), mate discrimination should increase. If result either in a genetic contribution to offspring (in the this is indeed the case, and if males are able to discriminate case of copulation with a parthenogen) or in fertile and/or against parthenogenetic females, the parthenogens should viable offspring at all (heterospecific or sterile mating receive fewer copulations when present at high frequen- partners). cies. In this situation, parthenogens that are dependent Biological conditions under which mate discrimination upon copulatory stimuli to maximize reproductive output may be important are not hard to come by. One obvious will be at a competitive disadvantage relative to their example, as discussed above, is provided by the 50 or sexual counterparts. so pseudogamous ‘species’ coexisting with their sexual These theoretical predictions are supported by several progenitors that reproduce clonally but require sperm studies demonstrating that frequency-dependent male dis- from a male from a closely related species to initiate crimination against parthenogenetic females does occur. embryogenesis (Dawley 1989; Go´mez & Serra 1996; McKay (1971) determined that pseudogamous topmin- Schlupp & Ryan 1996). Other situations where the evolu- nows (Poeciliopsis spp.) receive more copulations when tion of discriminatory mating behaviour may be fav- male densities are high, most likely because competitive oured include mollusc populations afflicted by castrating interactions between males for sexual females relegate parasites and mixed sexualeparthenogenetic popula- smaller males to mating with pseudogamous females. The tions in which parthenogenetic females persist in mating frequency of inseminated pseudogamous females de- with male congeners despite the lack of need for sperm creases sharply as male frequency decreases. One study in any capacity (e.g. Crews et al. 1986; unpublished of fertilization rates in natural populations of mixed data). sexual/pseudogamous Poeciliopsis found that females from Despite its costs, males persist in engaging in copulatory clones common in a population were less likely to be behaviour with parthenogens (e.g. Woodhead & Armstrong fertilized than females from uncommon clones (Schultz 1985; Walker et al. 1991; Abt & Reyer 1993; Schlupp et al. 1982). Keegan-Rogers (1984) followed this study by show- 1994; Løyning & Kirkendall 1996). It follows that males ing that male Poeciliopsis lucida were more likely to that are able to discriminate between sexual and parthe- mate with pseudogamous Poeciliopsis hybrids from un- nogenetic females and avoid the costs of needless mating familiar clones than with pseudogamous females from behaviour and copulation should, under most circum- clones that had been reared with the males. She concluded stances, be selectively favoured. by suggesting that selection favouring males that learn to Researchers investigating mating behaviour in coexist- avoid familiar females may underlie the expression of ing sexual and parthenogenetic populations have shown discriminatory mating behaviour in P. lucida. A similar that mate discrimination does occur and is usually biased pattern was demonstrated by Woodhead & Armstrong towards sexual females (Table 1). Several early studies (1985), who found that male Poecilia latipinna learn to showed that male sailfin mollies, Poecilia latipinna, are able avoid pseudogamous Poecilia formosa, mating indiscrim- to discriminate between sperm-dependent pseudogamous inately when young, but exclusively copulating with females and sexual females, mating only with gynogens sexual females when mature (Woodhead & Armstrong when all sexual females have been mated (Hubbs 1964; 1985). McKay 1971; Keegan-Rogers 1984). More recently, Ryan There is also evidence from invertebrate populations for et al. (1996) and Gabor & Ryan (2001) examined mating frequency-dependent male discrimination against less behaviour in a related pseudogamous/sexual molly species desirable females. Lawrence (1986) found that male milk- complex, the sexual Poecilia mexicana and P. latipinna and weed , Tetraopes tetraopthalmus, are more discrimi- the pseudogamous P. formosa, and showed nating of potential mates when there are more females that males from both sexual species also discriminate from which to choose, preferentially selecting larger, more against the pseudogamous forms, particularly when the fecund females as the sex ratio becomes more female males are from populations sympatric with parthenoge- biased. Løyning & Kirkendall (1996) discovered that the netic females. ability of male bark beetles to discriminate between sexual In coexisting populations of sexual and parthenogenetic and parthenogenetic females is dependent on genotype, invertebrates, ‘conspecific’ males have also been shown to with certain clones being able to obtain copulations at display mate discrimination against female parthenogens. a much higher rate than others. In addition, the authors The best example of this phenomenon is that provided by noted that male experience influences the likelihood that Løyning & Kirkendall (1996), who examined mating parthenogenetic females will receive copulations; males behaviour in a complex of the coexisting sexual and that have been exposed to parthenogenetic females are pseudogamous bark beetle, Ips acuminatus, and showed better able to discriminate between sexual and partheno- that males prefer to mate with sexual females. genetic females than are naı¨ve males. REVIEW 817

Spatial separation of parthenogenetic females and males successfully with related sexual competitors across a het- Parthenogenetic females might not receive adequate erogeneous environment and seem to be more closely copulations because parthenogens and males use different adapted to particular niches than are sexual individuals. resources or microhabitats. Even if males do not actively On the far end of the spectrum of ecological differen- discriminate against copulating with parthenogenetic tiation are asexual taxa that thrive in habitats that are females, differential habitat or resource use by sexual entirely outside of the ranges of closely related sexual and parthenogenetic individuals could decrease the prob- species. This phenomenon suggests that copulatory de- ability that parthenogenetic females will encounter males. pendence does not always constitute an absolute barrier to A relevant perspective on this issue is provided by parthenogenetic success, especially if selection favouring Stenseth et al. (1985), who modelled the effects of spatial parthenogenetic females that are less reliant on copulato- separation between coexisting subpopulations of pseu- ry stimuli can manage to erode physiological coupling dogamous and sexual individuals on copulation frequen- between copulation and offspring production. cy and the maintenance of sex. Under the assumption While there is no direct evidence for a genetically based that pseudogamous access to copulation decreases with decoupling of the physiological link between copulatory increasing spatial separation between the two types of stimuli and reproduction in parthenogenetic populations, individuals, greater spatial separation increases the likeli- the ecological success of the parthenogenetic Cnemido- hood of the maintenance of sex. As discussed above, in phorus lizards, as discussed above, does suggest that physio- situations where there is complete dependence of pseu- logical reliance on copulatory stimuli may have decreased dogamous females on sperm, the maintenance of sex is following the derivation of the parthenogenetic lizards not as paradoxical as it is in situations where true from their sexual ancestors. This possibility should be parthenogens and sexuals coexist. However, the Stenseth examined experimentally. et al. study is analogous to the ideas presented here in that spatial separation between sexual and pseudogamous species decreases the otherwise two-fold advantage of DISCUSSION parthenogenetic reproduction. Many studies have found some evidence for ecological The documented dependence of both sexual and parthe- differentiation between sexual and parthenogenetic indi- nogenetic organisms on the physiological stimulation viduals of the sort that could result in limited contact provided by copulation suggests that the success of a between parthenogens and males (Table 1). Indirect parthenogenetic strategy may be limited by access to support for this possibility is provided by several studies males and their willingness to copulate. Even if offspring of vertebrate, invertebrate and parthenogenetic taxa production is only slightly reduced in the absence of that have shown the presence of interclonal variance for copulation, some degree of copulatory dependence could ecologically relevant traits such as feeding morphology still aid in maintaining sex. Copulatory dependence could and behaviour (Browne 1992; Weeks et al. 1992; Geedey be particularly relevant to the maintenance of sex if the et al. 1996; Butlin et al. 1998; Weeks & Hoffman 1998; decrease in fecundity in parthenogenetic females caused Negovetic & Jokela 2000) or spatial separation of different by lack of access to copulations is compounded by other, clonal genotypes into different habitats (Stratton 1991, more long-term issues related to asexuality, such as sus- 1994; Geedey et al. 1996). Although interclonal differen- ceptibility to deleterious mutation accumulation and the tiation per se does not constitute definitive evidence inability to generate genetically rare or novel offspring that sexual and parthenogenetic individuals inhabit dif- (West et al. 1999). ferent areas or use different resources, it does show that The possibility that dependence on copulation could asexual taxa can display some degree of niche specificity. exact a cost of parthenogenetic reproduction is supported These data indicate that the variance required for the fine- by the empirical work reviewed above. Many studies on scale niche partitioning that may result in limited a wide variety of animal taxa have shown that maximal copulatory opportunities for parthenogenetic females is reproductive output requires copulatory stimuli. The present. small body of work examining the relation between A few studies have provided more direct evidence for copulation and offspring production in parthenogens is ecological differentiation between sympatric parthenoge- also promising, suggesting that parthenogenetic females netic and sexual individuals. Løyning (2000) described may often retain some functional dependence on copu- ecological differentiation between sexual and partheno- lation in order to attain full reproductive potential. There genetic forms of the bark beetle I. acuminatus. Similarly, is also evidence that mechanisms such as active male Booij & Guldemond (1984) and Kovel & de Jong (2000) discrimination and spatial separation may often limit found, respectively, that pseudogamous and sexual plan- access of parthenogenetic females to copulation. However, thoppers (Muellerianella spp.) and dandelions (Taraxacum although copulatory dependence is a theoretically viable spp.) use different ecological resources. mechanism for the maintenance of sex, more information The most definitive evidence for asexual ecological on the presence and consequences of courtship behaviour differentiation and spatial separation comes from work on and copulation of parthenogenetic females in natural parthenogenetic lineages of woodlice and oligochaete populations is needed to determine whether this mech- worms (Christensen et al. 1992), brine shrimp (Browne anism may in fact act to aid the maintenance of sex. These 1992) and mites (Weeks & Hoffman 1998). These authors data are only available for a tiny fraction of parthenoge- all showed that the parthenogenetic lineages compete netic species. 818 ANIMAL BEHAVIOUR, 67, 5

Knowledge of whether there is copulatory dependence between copulatory stimuli and reproduction in a re- and whether copulation occurs in a wide variety of asexual cently derived parthenogen is provided by the work of taxa will allow more direct determination of whether this Carson et al. (1982) and Crews et al. (1985). These mechanism can help to maintain sex. In particular, these researchers examined mating behaviour and reproduc- data will show whether the frequency of sexual indi- tion in the sexual fly D. mercatorum and in viduals both within and between species varies with the parthenogenetic fruit fly lines derived 20 years ago from degree of asexual copulatory dependence and access to D. mercatorum. Maximal egg production in the sexual copulation. females was found to be reliant on courtship and If copulatory dependence is an important mechanism copulatory stimuli (Crews et al. 1985). However, despite contributing to the maintenance of sex, we would expect a marked decay in the expression of mating behaviour in the degree of a sexual copulatory dependence to have the parthenogenetic females relative to the sexual females predictable relationships with access to copulations and (Carson et al. 1982), the parthenogens still produced eggs the frequency of sex both within and between species. In at a rate equivalent to the sexual females (Crews et al. particular, there should be a positive correlation between 1985). Carson et al. cited the decay of mating behaviour in the degree of asexual copulatory dependence and the the parthenogenetic flies as potential evidence for the frequency of sex. In addition, given some degree of accumulation of that functionally depress copulatory dependence, there is likely to be a higher mating behaviour. frequency of sexual individuals in populations/species in The possibility that copulatory dependence might pro- which males either discriminate against parthenogenetic vide an advantage to sexual reproduction is also intriguing females or are ecologically and/or spatially separated in that it is likely to provide an advantage to sex relatively from them. soon after a transition to asexuality. A short-term ad- If phylogenetic constraints do result in the retention of vantage to sex is not provided by most genetically based parthenogenetic dependence on copulation, the degree of mechanisms for the maintenance of sex, which often do dependence may also vary in a predictable manner. In not begin to provide a substantial benefit to sexual particular, there may be a relationship between the degree reproduction until many generations following the in- of dependence and both time since divergence of parthe- vasion of an asexual mutant (Howard & Lively 1994). nogenetic taxa from their most recent sexual ancestor and Thus, the potential applicability of a mechanism that can the degree of asexual access to copulations. reduce parthenogenetic fitness immediately following Thus, if copulatory dependence is a mechanism that a transition to asexuality is an important addition to the contributes to the maintenance of sex, successful (i.e. group of mechanisms focused around the maintenance of extant) parthenogenetic taxa that do thrive without en- sex, particularly when considered in combination with countering males may be those taxa that were lucky other mechanisms that act to maintain sex over longer enough to experience the genetic and/or developmental periods of evolutionary time (West et al. 1999; Simon et al. changes that would increasingly decouple reproduction 2002). from copulatory behaviour. To elaborate further, if there is Ultimately, the aim of this review was to address one of heritable for dependence on copulation the most important and contentious unanswered ques- between asexual females, selection will favour asexual tions in evolutionary biology today, that of the nature of females that are less dependent on stimuli from males, the mechanism(s) that underlie the seemingly paradoxical particularly if males are discriminatory or are rarely widespread occurrence of sex. I suggest that a largely encountered. However, it is unlikely that alleles decreasing ignored mechanism, that of evolutionary constraints sexual female dependence on copulatory stimuli would imposed on parthenogenetic females recently descended have been segregating in the sexual progenitor popula- from sexual ancestors, could act alone as a short-term tion, because these ancestral females would have neces- facilitator of the maintenance of sex, or in concert with sarily been dependent on sperm, and thus, on copulation other, genetically based mechanisms to maintain sex over (see Carson et al. 1982). This means that the ability of evolutionary time. A wide body of evidence indicates that asexual females to escape dependence on copulation will parthenogenetic females may in fact retain elements of be a function of the rate of mutation to a less dependent a reproductive physiology that were beneficial to sexual reproductive physiology following their derivation from ancestors but could act to depress the evolutionary sexual populations. Once these alleles arise, they should potential of parthenogenetic lineages. be heavily favoured, particularly if parthenogen access to If future research does support the possibility that the males is limited. full realization of reproductive potential in parthenoge- Based on this reasoning, asexual dependence on netic females is dependent on copulatory stimuli, and that copulatory stimuli should decrease both with increasing parthenogenetic females do not always receive enough time since derivation from the sexual progenitor species copulatory stimulation to reproduce at maximal levels, and with decreased access of asexual females to males, then the widespread distribution of sexual reproduction such that parthenogens from populations/species that may not be wholly due to selective advantages of sexual rarely or even never encounter males may show less reproduction, as has generally been assumed. Rather, the copulatory dependence than do females from popula- current predominance of sex could in part be more simply tions/species that do coexist with males. ascribed to evolutionary constraints preventing partheno- Evidence supporting or refuting these predictions genetic females from fully realizing the benefits of is nearly nonexistent. A lone example of decoupling producing all-female offspring. REVIEW 819

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