DOI: 10.1111/eea.12000 SPECIAL ISSUE: FEMALE MATING FAILURES Mating failures as a consequence of sexual selection on females Darryl T. Gwynne1*&PatrickD.Lorch2 1Department of Biology, University of Toronto in Mississauga, Mississauga, Ontario, L5L 1C6, Canada, and 2Biological Sciences Department, Kent State University, 256 Cunningham Hall, Kent, OH 44242, USA Accepted: 18 June 2012

Key words: female competition, , Diptera, , , katydids

Abstract Multiple mating by individuals successful in sexual competition results in other individuals failing to mate. This leads to sexual selection within a sex, typically the males. However, more are com- ing to light in which females are subject to sexual selection. We review the contexts for and nature of sexual selection on females in several species where female mating failures have been noted. We then examine evidence of mating failures in two groups of , empidid flies (Diptera) and tettigoniid Orthoptera (katydids), in which sexual selection is expected to be relatively stronger on females. Using data from the field, we show for two species of katydids that, as predicted, there are mating failures by females in populations in which the direction of sexual selection appears to be reversed, but not in populations where sexual selection appears to be stronger on males.

investment in paternal care or other benefits that limit the Introduction potential rate at which females can reproduce (Thornhill, In polygynous species, multiple matings by some males 1986; Clutton-Brock & Vincent, 1991). More rarely, a leaves others unmated, thus imposing sexual selection on female-biased OSR, and thus a role reversal, occurs when this sex (Darwin, 1871; Eberhard, 1996). This class of there is a bias in the primary sex ratio typically caused by unmated males is an important source of sexual selection, high mortality among males (Jiggins et al., 2000). Sexual having a greater effect on variation in male reproductive competition among females can also co-occur with male– success than variation in the number of matings with dif- male competition when the competition is for the best ferent females within the fraction of successfully mating males (Kokko & Jennions, 2008). males (Shuster & Wade, 2003; Shuster, 2011). Estimates of The quantification of mating failures in females is easier mating variance are commonly used to gauge the opportu- than in males because the detection of the ‘zero class’ males nity for sexual selection within a sex (Krakauer et al., 2011; in nature can be difficult (Shuster & Wade, 2003), espe- but see Lorch, 2005; Jennions et al., 2012). cially if these loser males have retreated from locations Although sexual selection is typically associated with where most of the mating competition and copulations males, more species are coming to light in which females are observed. Detection of mating in females, especially in are subject to this powerful form of selection as, for exam- insects, is straightforward for most species, because dissec- ple, imposed by male choice of mates (found in many taxa: tion of females reveals mating evidence such as the pres- Bonduriansky, 2001). Intense sexual selection on females ence of sperm in storage organs (Rhainds, 2010). appears to occur in systems with reversals in the mating Here, we examine the evidence that mating failures roles, i.e., in addition to male mate choice, there is sexual among females are associated with sexual selection on competition among females when there are more of them females. First focusing on the hypotheses suggested by than males available for mating (Gwynne, 1991). Typically, Rhainds (2010) for mating failures in females, we discuss this bias in the operational sex ratio (OSR) is due to male as to what extent the evidence of failures can be linked to some form of sexual selection on females. We then exam- ine several species of dance flies (Diptera: Empididae) and *Correspondence: Darryl T. Gwynne, Department of Biology, katydids (Orthoptera: Tettigoniidae) for which there is University of Toronto in Mississauga, Mississauga, ON, Canada, behavioural or other evidence for a reversal in the L5L 1C6. E-mail: [email protected] direction of sexual selection (role reversal). In examples

© 2012 The Netherlands Entomological Society Entomologia Experimentalis et Applicata 146: 3–10, 2012 Entomologia Experimentalis et Applicata © 2012 The Netherlands Entomological Society 3 4 Gwynne & Lorch from these groups, we examine the evidence that female combination with other factors – may promote sexual mating failures are associated with losing in the competi- selection among females. For example, a field study of tion for mates. In particular, we focus on two species of sessile females of the monandrous psychid Metisa katydids in which a greater proportion of female mating plana Walker over five generations revealed that 7–18% of failures is expected in populations showing behavioural females are uninseminated. In most generations, there was role reversal than in other populations of the same species a strong sex ratio bias towards females which appeared to for which the mating roles are typical. result in sexual selection on females and thus female mating failure. There was some evidence of male mate choice and also of signal interference between females; attractive pher- Sexual selection omonesfrom certain(e.g., large)females appear to interfere Sexual selection is defined here in the original Darwinian with the ability of other individuals to attract males sense as selection in the context of competition for mates (Rhaindset al.,1999).This iseither a formofpassiveattrac- (Shuker, 2010). This is generally understood to be compe- tion (Arak, 1988) ofmales to the most prominent signal of a tition to increase mating frequency. The mating frequency group of non-interacting females (the usual case in ; component of competition for mates turns out to be more Lim & Greenfield, 2008) or a more active form of choice of relevant for females than for males, for whom post-copula- certain females by males (probably more likely when tory competition between different males within a female females increase signalling effort in response to nearby explains a large amount of variance in reproductive competitors – e.g., the arctiid moth Utetheisa ornatrix L., success. Post-copulatory sexual selection in males includes in which females appear to be competing for nutritious direct competition between ejaculates (sperm competi- male spermatophores; Lim & Greenfield, 2007). Impor- tion) and cryptic female choice such as allocation of tantly, however, even passive attraction still imposes sexual resources to zygotes sired by preferred males (Eberhard, selection onfemales for certain traits such as body size. 2009). In females, on the other hand, fitness gains often When there are local high densities of females, mating come from increasing mating frequency. This is particu- failures are also possible in other sorts of mating groups. larly true for females of species in which males provide In butterflies that are attracted to lekking sites, there is a goods and services (e.g., nuptial gifts of food and paternal higher incidence of unmated females compared to other care). For example, in role-reversed insects, copulations sites (Shields, 1967; cited in Rhainds, 2010). In this system, that failed to inseminate still provided nuptial meals that virgin females may be losers in sexual competition for the can enhance female fitness (Gwynne, 1993). So, at least in best mates. In fact, a study of a lekking antelope Damalis- systems where males contribute gifts or care, post-copula- cus lunatus (Burchell) (Bro-Jorgensen, 2002) revealed that tory sexual selection among males may mean that females female fights are most common at the lek centre and gain more fitness than males can by mating with addi- females in these locations are also more likely to disrupt tional mates (Lorch, 2002). matings than elsewhere in the lek area. This is a case in In addition to fitness advantages due to mating with which there is both sexual competition between males (for multiple mates, both males and females should gain fitness occupation of central lek territories) and between females by mating with (or favouring through post-copulatory (for the best mates). Thus there is sexual selection on both mechanisms) higher quality mates (Thornhill, 1986). For sexes. this reason we will consider competition both for more Sexual selection on females is also likely when there is mates and for better mates in our definition of sexual variation in emergence times of receptive females, or in the selection. Both types of competition can result in unmated arrival times of females when their sexual receptivity females. Note that the competition for mates definition occurs after migration. Females that synchronize their used here contrasts with that of recent reviews that dilute emergence with the time when most males are available the concept of sexual selection on females to include any have the highest mating success (e.g., several lepidopter- sort of social competition to reproduce (Clutton-Brock, ans: Rhainds, 2010). Females of monandrous species that 2007, 2009; Shuker, 2010). emerge too early as adults, when female emergence precedes that of males (protogyny), run the risk of going unmated because limited numbers of males are available Sexual selection and female mating failures (Rhainds et al., 1999). A similar situation may occur for Rhainds (2010) outlined a list of circumstances in which late emergers in protandrous species or late arrivals in sexually receptive females fail to mate. Most of the hypo- species with females that migrate before mating (Rhainds, theses can be related to some form of sexual selection on 2010). Late individuals will also suffer decreased fitness if females. First is failure to mate when local densities – in the quality of the remaining available males is low. This Female mating failures and sexual selection 5 type of sexual selection was first suggested by Darwin care; see Jones et al., 2005) can be both sufficiently costly (1871) to explain sexual selection in sexually dimorphic to males and important to female fitness that the OSR is monogamous birds. He argued that early arriving males biased towards females. This produces a reversal in the gained an advantage by pairing with high condition early- direction of sexual selection on the sexes (Gwynne, 1984a, nesting females (Kirkpatrick et al., 1990). If there is sexual 1991; Thornhill, 1986; Parker & Simmons, 1996). Our selection on females in monandrous species (Rhainds insect examples are certain species of katydids (Ortho- et al., 1999), the selection is generated to a large extent by ptera: Tettigoniidae) and some dance flies (Diptera: Empi- the difference in fitness between individuals who have and didae) with highly nutritious nuptial gifts that are eaten by have not mated (Shuster & Wade, 2003; Shuster, 2011). females during insemination. In the empidids the meal is Finally, a common suggestion for female mating failures prey and in katydids a large glandular mass (attached to that is not a consequenceofsexualselectionis the low rate of the spermatophore) that the female removes and eats after encounter with mating partners expected at low population mating. In both groups there is evidence of a reversal in densities (exacerbated with certain life histories such as the mating roles: females compete for access to males and flightless females).There are naturally selected femaleadap- their gifts and males are choosy when mating. Evidence of tations in response to such situations (Rhainds, 2010) such mating failures in these insects is reported in Table 1. asreducingriskandthusincreasinglifespan[e.g.,virginixo- did ticks attached to hosts that avoid detection by hosts by Searching for mates not engorging with blood until after their single mating (monandry); Kaufman, 2007]. However, sexually selected Sexual selection for female mate searching in Tettigoniidae adaptations to low rates of encountering mates, especially was recently investigated by McCartney et al. (2011). when population densities are low, are expected to raise the Searching for mates is typically a sexually selected male mating success of some females. Rhainds (2010) lists active trait – a risky way of increasing mating success (Darwin, searchingformates,aggressionbetweenfemales,andextrav- 1871; Alexander & Borgia, 1979; Thornhill, 1979). Within agant female traits, the ornamental ‘secondary sexual char- the katydid genus Poecilimon there is variation in pair- acters’ (Darwin, 1871) that attract mating partners. All have formation protocols: in some species males search for sing- been studied recently in nuptial-feeding insects in which ing females, whereas in others, females move towards male thereis a reversal in the direction ofsexual selection. Wewill callers. McCartney et al. (2011) tested the hypothesis that coverallthreeintheremainingsectionsofthispaper. female mate searching evolves in species with large (and likely more nutritious) spermatophore gifts as females in these species should have experienced more intense sexual Mating failures and sexual selection on females in selection than species with small gifts. Male mate searching species with nuptial gifts is ancestral in the genus Poecilimon and a comparative test We focus on species in which males provide important supported the prediction that significantly larger gifts nuptial meals to their mates. Valuable gifts (or paternal evolve in species in which female searching was

Table 1 Percentage of mating failures by females in several species in which there is evidence of sexual selection on females (see text) medi- ated by group signalling (a psychid moth) or sexual competition when there are reversals in the mating roles (empidid flies and tettigoniid orthopterans). For two species of Tettigoniidae, mating rates are compared between role-reversed populations and populations with typical roles (i.e., no apparent sexual competition between females)

Nature of sexual %matingfailure Order Species selection by females Reference Lepidoptera Metisa plana Group signalling by females 7–18 (several Rhainds et al. (1999) generations) Diptera Role reversal; female swarms 36 (n = 36) Svensson (1997) marginata R. longicauda Role reversal; female swarms 6 Wheeler et al. Orthoptera simplex Role reversal; hungry females compete for gifts 3 (n = 95) Gwynne (1993) Typical roles; no female competition 1 (n = 79) Gwynne (1993) Metaballus litus Role reversal; hungry females compete for gifts 11 (n = 73) Gwynne (1985) Typical roles; no female competition 0 (n = 13) Gwynne (1985) 6 Gwynne & Lorch evolutionarily derived. For Poecilimon it is unclear to what ming, 1994). Despite the potential cost to fecundity of these extent role reversal in mate searching is accompanied by a elaborate female traits, they may be important when fecun- reversal in the direction of sexual selection, i.e., a full rever- dity cannot be assessed directly by males, e.g., when signals sal in the mating roles. offemalefecundity are necessaryunder low light conditions in which all-female swarms are known to occur (Funk & Tallamy,2000;Chenowethet al.,2006). Aggression between competing females One feature of several groups of showing reversals Mating failures in dance flies and katydids in the direction of sexual selection is direct aggression or other forms of intrasexual competition between sexually Given the tettigoniid and empidid examples of role rever- competing females. This is typically an adaptation to gain sal where there is measurable sexual selection on females access to multiple mates and the resources they supply and (Bussie`re et al., 2008; Robson & Gwynne, 2010; Wheeler includes female domination of others or fights between et al., 2012), we expect female mating failures due to the females for access to parental males in some birds, frogs, high levels of sexual competition between females in role fishes, and harvestmen (Opiliones; Table 9-1 in Gwynne, reversed populations. Two studies have reported high rates 2001). In our role-reversed insect systems, the competition of mating failures in Rhamphomyia empids (Svensson, is for nuptial gifts. Species with valuable nuptial gifts 1997; Funk & Tallamy, 2000; Table 1), but these data, include empids that form all-female competitive swarms based on spermathecal dissections, were not obtained at attractive to males bearing nuptial prey (Svensson, 1997; the end of the reproductive season and therefore it remains Funk & Tallamy, 2000) and katydids in which there are possible that virgin females were recently emerged individ- fights between females for males and their nutritious gifts uals rather than losers in the intense sexual competition (Gwynne, 2001). The reversal in the direction of sexual for matings within swarms. However, as mentioned above, selection in these insects appears to be driven by the critical mistiming of emergence by adult females can still result in importance of male mating gifts to female reproduction. In sexual selection if, for example, late emergers mate less the flies (some species of Rhamphomyia and Empis), pro- often and thus obtain fewer nuptial meals. Further research teinaceous food necessary for egg production comes solely with empid species would be useful, particularly if sex from male gifts and opportunities to mate and feed can be role-reversed species are compared to species with more very limited; e.g., just a couple of hours of mating swarms typical roles (e.g., those with all-male swarms; Funk & each day in two Rhamphomya species, where gift-laden Tallamy, 2000), with the prediction of fewer female mating males ascend through swarms and reject smaller females as failures in the latter species. mates (Svensson, 1997; Funk & Tallamy, 2000). In katy- This prediction can be tested intraspecifically in katydid dids, a scarcity of proteinaceous food – e.g., at high popula- species in which there are both role-reversed populations tion densities – skews the OSR towards an excess of females and populations with more typical roles. Field studies of because there are fewer spermatophore gifts produced by the Mormon , Anabrus simplex Haldeman, and starved males and because hungry females are more pro- Metaballus litus Rentz provide support (Table 1, miscuous as they forage for frequent matings (gifts). In Figure 1). In these tettigoniine katydids, the number of these populations, females encountering each other en matings achieved by females can be determined from sper- route to calling males often fight, and males reject smaller, mathecal dissections. Following each mating, a separate less fecund females as mates (review in Gwynne, 2001). spermatodose is formed within the spermatheca (Gwynne, 1984b; Vahed, 2003). For A. simplex there were female mating failures in two role-reversed populations (in which Exaggeratedtraitsinfemales the species forms large aggregations), but not in the popu- The exaggerated traits typical of males in many animals are lation in which the mating roles were typical: males were rare in females of role-reversed species. The scarcity of observed to compete and females to choose mates female ornaments may be a consequence of trait cost. That (Gwynne, 1984b). The most appropriate comparison is is, fecundity limits female investment in ornaments, and between the role-reversed and populations with typical malesseekingthemostfecundfemalescould,forthisreason, roles sampled at the peak of the season in the same year evenavoidfemaleswithexaggeratedtraits(Fitzpatricket al., (Figure 1, Antelope Flats and Indian Meadows). A similar 1995).Empidinedancefliesareexceptionalinthatover25% lack of mating failures when roles are typical (and mating of species appear to have female ornaments including large failures with role reversal) was found for the Australian wings, elaborate tibial scales, and abdominal pouches that katydid M. litus (Figure 1), in the same year at mid- are inflated just prior to entering the mating swarm (Cum- season. Observations in the wild on the flexible mating Female mating failures and sexual selection 7

Role reversed Anabrus Role reversed Metaballus Antelope Flats, UT, USA 1981 Dunsborough, Australia 1981

15 30 25

10 20 15

5 10 5

0 0 02468101214 02468101214

Typical role Anabrus Typical role Metaballus Indian Meadows, CO, USA 1981 Buayanup, Australia 1981 7 4 6 5 3 4 2 3 Count 2 1 1 0 0 0 2 4 6 8 10 12 14 02468101214

Role reversed Anabrus Polson, MT, USA 1990 25

20

15 Figure 1 Female mating frequencies in nature for two species of katydids 10

(Orthoptera: Tettigoniidae) comparing 5 populations with typical roles (sexual selection on males) to those with reversed 0 roles (sexual selection on females). Note 02468101214 that the axes are not standardized. Female mating frequency

Ad libitum food Anabrus Food deprived Anabrus behaviour of A. simplex (Gwynne, 1981, 1984b) were fol- Polson, MT, USA 1990 Polson, MT, USA 1990 lowed by experiments using field enclosures to demonstrate 50 50 that food limitation created an excess of females seeking 40 40 mates, and thus a reversal in the mating roles (Figure 2). In contrast to field results, there were some females that failed 30 30

to mate in the populations showing typical roles (enclo- Count 20 20 sures with ad libitum food). However, as expected, more females failed to mate in role-reversed (food-deprived) 10 10 enclosures (figure 2) (Gwynne, 1993). Consistent with the 0 0 results for species with typical roles, in another katydid, 012345 012345 roeselii (Hagenbach), all 36 virgin adult females Female mating frequency released and recaptured after about a week had mated Figure 2 Female mating frequencies from field enclosures for (Kindvall et al., 1998). It is unlikely that there is any sexual Anabrus simplex. Enclosures in which the insects were food competition between females in this species given its habi- deprived showed reversal in the mating roles and significant tat, low population density, and food availability. sexual selection for larger females. Enclosures with ad libitum The range of female mating failures in natural popula- food showed typical mating roles and no sex difference in sexual tions of role-reversed katydids and empid flies (3–33%; selection for body size. 8 Gwynne & Lorch

Table 1) is less than the 55% observed for a well-studied compared to the opposite sex (true even in very large system showing sex role reversal, the pipefish Syngnathus populations). Thus, OSR will covary with the variance scovelli (Evermann & Kendall) (Jones et al., 2001). In syn- estimate even when there is no change in actual intensi- gnathid fishes (pipefishes and seahorses), females deposit ties of sexual selection. eggs in the male’s brood pouch and in several pipefishes Darwin’s (1871) ideas about sexual selection were this elaborate male parental care is associated with com- inspired by real traits and Jennions et al. (2012) recom- petitive, brightly coloured males and choosy females mend ‘quantifying actual sexual selection on traits of inter- (Berglund & Rosenqvist, 1993). est’. For the enclosure study with the katydid A. simplex (Gwynne, 1993), a female trait of interest is body size because choosy males appear to assess the weights of Discussion females that mount them; they reject small, less fecund Discussions of sexual selection have highlighted the class individuals (Gwynne, 1981). Simple correlations between of loser individuals in two related ways: first, in polyga- female size and the frequency at which they were observed mous species with equal sex ratios are individuals within to mate supported the prediction of a significantly positive the competing sex that remain unmated (Darwin, 1871), correlation only in food-deprived (role-reversed) enclo- and second, this ‘zero-mating’ class of individuals has a sures (for the ad libitum food enclosures there was no stronger influence than other mating classes on variance- significant correlation; Gwynne, 1993). In this study it was based estimates of the opportunity for sexual selection on interesting to note that there were no significant correla- a sex (Shuster & Wade, 2003). Accurate measures of sexual tions (for either of the food enclosure treatments) between selection are important for testing predictions such as: a female’s size and a second measure of her fitness, her (1) in species with behavioural reversals in the mating insemination success. This is the measure reported above roles, the direction of sexual selection is reversed, i.e., the (Table 1, Figure 1) for A. simplex and M. litus, and esti- intensity of sexual selection on females exceeds that of mated by the number of spermatodoses (sperm capsules) males; and (2) in species in which the direction of sexual within the spermatheca. The discrepancy between the two selection varies between populations, sexual selection on measures could well be due to the high insemination failure females should be greater in populations showing role rate – 21% of the females from enclosures had more reversal than in populations with typical mating roles. observed matings (i.e., spermatophores transferred and The first prediction has support from three vertebrates; thus nuptial gifts eaten) than spermatodose counts. This variance in female mating success exceeds that of males in was comparable to 33% of laboratory matings (and similar the pipefish S. scovelli and two role-reversed birds (with rates in other katydids; Lorch et al., 2008) that resulted in exclusive paternal care), the spotted sandpiper and the spermatophore (gift) transfer but no insemination. Failure bonze wing jacana (Jones et al., 2001). For the second to inseminate probably occurs because of improper inser- prediction, a variance-based measure of the opportunity tion of the spermatophore into the female’s genital cavity. for sexual selection (variance/mean mating frequency) However, it is also possible that, because the male has little revealed a significantly higher value for food-deprived direct control over insemination (insemination from the enclosures (role reversal) than for enclosures with ad libi- spermatophore taking place after ), females tum food in the katydid Kawanaphila nartee Rentz (a may adaptively block insemination by some males while third species showing plasticity in the mating roles; fully consuming their nuptial gifts. Gwynne & Simmons, 1990), but not for a comparison of We have demonstrated that mating failures are associ- enclosures with similar food treatments in the katydid ated with competition for mates in females of some A. simplex (Gwynne, 1993). However, variance-based species, particularly when female fitness increases with the measures of sexual selection are problematical (see dis- number of mates due to nuptial gifts. In these species, the cussion by Lorch, 2005; Klug et al., 2010; Krakauer et al., number of gifts eaten is almost certainly more important 2011; Jennions et al., 2012). Variance measures are typi- than the success in receiving sperm-filled spermatodoses cally regarded as estimates of the opportunity for sexual (each delivers sufficient sperm in the millions; Gwynne, selection (Shuster & Wade, 2003). However, Jennions 2001). Because insemination success is more important to et al. (2012) question the utility of these measures even as male than to female fitness in these species, failure to estimates of the opportunity or upper limits on sexual inseminate has different effects on the upper limit of sexual selection. They point to the strong contribution of selection on each of the sexes (Lorch et al., 2008). Thus, random events to variation in mating success (see also mating success is the critical parameter in understanding Sutherland, 1987). When OSRs are strongly biased the patterns of sexual selection on females in species in number of the sexually competitive sex is very large which males supply valuable gifts or paternal care. Female mating failures and sexual selection 9

References Gwynne DT (1984b) Sexual selection and sexual differences in Mormon crickets (Orthoptera: Tettigoniidae, Anabrus Alexander RD & Borgia G (1979) On the origin and basis of the simplex). Evolution 38: 1011–1022. – male female phenomenon. Sexual Selection and Reproductive Gwynne DT (1985) Role-reversal in katydids: habitat influences Competition in the Insects (ed. by M Blum & N Blum), pp. reproductive behaviour (Orthoptera: Tettigoniidae: Metaballus – 417 440. Academic Press, New York, NY, USA. sp.). Behavioral Ecology and Sociobiology 16: 355–361. Arak A (1988) Female mate selection in the natterjack toad: active Gwynne DT (1991) Sexual competition among females: what choice of passive attraction? Behavioral Ecology and Sociobiol- causes courtship-role reversal? Trends in Ecology & Evolution – ogy 22: 317 327. 6: 118–121. Berglund A & Rosenqvist G (1993) Selective males and ardent Gwynne DT (1993) Food quality controls sexual selection in females in pipefishes. Behavioral Ecology and Sociobiology 32: Mormon crickets by altering male mating investment. Ecology – 331 336. 74: 1406–1413. Bonduriansky R (2001) The evolution of male mate choice in Gwynne DT (2001) Katydids and Bush-crickets: Reproductive insects: a synthesis of ideas and evidence. Biological Reviews Behavior and Evolution of the Tettigoniidae. Cornell Univer- – 76: 305 339. sity Press, Ithaca, NY, USA. Bro-Jorgensen J (2002) Overt female mate competition and Gwynne DT & Simmons LW (1990) Experimental reversal of preference for central males in a lekking antelope. Proceedings courtship roles in an insect. Nature 346: 172–174. – of the National Academy of Sciences of the USA 99: 9290 Jennions MD, Kokko H & Klug H (2012) The opportunity to be 9293. misled in studies of sexual selection. Journal of Evolutionary Bussie`re LF, Gwynne DT & Brooks R (2008) Contrasting sexual Biology 25: 591–598. selection on males and females in a role-reversed swarming Jiggins FM, Hurst GDD & Majerus MEN (2000) Sex-ratio- dance fly, Rhamphomyia longicauda Loew (Diptera: Empidi- distorting Wolbachia causes sex-role reversal in its butterfly – dae). Journal of Evolutionary Biology 21: 1683 1691. host. Proceedings of the Royal Society of London B 267: 69–73. Chenoweth SF, Doughty P & Kokko H (2006) Can non-direc- Jones AG, Walker D & Avise JC (2001) Genetic evidence for tional male mating preferences facilitate honest female orna- extreme polyandry and extraordinary sex-role reversal in a – mentation? Ecology Letters 9: 179 184. pipefish. Proceedings of the Royal Society of London B 268: Clutton-Brock T (2007) Sexual selection in males and females. 2531–2535. – Science 318: 1882 1885. Jones AG, Rosenqvist G, Berglund A & Avise JC (2005) The Clutton-Brock T (2009) Sexual selection in females. Animal measurement of sexual selection using Bateman’s principles: – Behaviour 77: 3 11. an experimental test in the sex-role-reversed pipefish Syngna- Clutton-Brock TH & Vincent ACJ (1991) Sexual selection and thus typhle. Integrative and Comparative Biology 45: 874–884. the potential reproductive rates of males and females. Nature Kaufman WR (2007) Gluttony and sex in female ixodid ticks: – 351: 58 60. how do they compare to other blood-sucking ? Cumming JM (1994) Sexual selection and the evolution of dance Journal of Insect Physiology 53: 264–273. fly mating systems (Diptera: Empididae; Empidinae). Cana- Kindvall O, Vessby K, Berggren A & Hartman G (1998) Individ- – dian Entomologist 126: 907 920. ual mobility prevents an allee effect in sparse populations of Darwin C (1871) The Descent of Man and Selection in Relation the bush-cricket Metrioptera roeseli: an experimental study. to Sex. John Murray, London, UK. Oikos 81: 449–457. Eberhard WG (1996) Female Control: Sexual Selection by Cryptic Kirkpatrick M, Price T & Arnold SJ (1990) The Darwin–Fisher Female Choice. Princeton University Press, Princeton, NJ, USA. theory of sexual selection in monogamous birds. Evolution 44: Eberhard WG (2009) Postcopulatory sexual selection: Darwin’s 180–193. omission and its consequences. Proceedings of the National Klug H, Heuschele J, Jennions MD & Kokko H (2010) The – Academy of Sciences of the USA 106: 10025 10032. mismeasurement of sexual selection. Journal of Evolutionary Fitzpatrick S, Berglund A & Rosenqvist G (1995) Ornaments or Biology 23: 447–462. – offspring costs to reproductive success restrict sexual Kokko H & Jennions MD (2008) Sexual conflict: the battle of the selection processes. Biological Journal of the Linnaean Society sexes reversed. Current Biology 18: R121–R123. – 55: 251 260. Krakauer AH, Webster MS, Duval EH, Jones AG & Shuster SM Funk DH & Tallamy DW (2000) Courtship role reversal and (2011) The opportunity for sexual selection: not mismeasured, deceptive signals in the long-tailed dance fly, Rhamphomyia just misunderstood. Journal of Evolutionary Biology 24: – longicauda. Animal Behaviour 59: 411 421. 2064–2071. Gwynne DT (1981) Sexual difference theory: Mormon crickets Lim H & Greenfield MD (2007) Female pheromonal chorusing – show role reversal in mate choice. Science 213: 779 780. in an arctiid moth, Utetheisa ornatrix. Behav Ecol 18: 165–173. Gwynne DT (1984a) Male mating effort, confidence of paternity Lim H & Greenfield MD (2008) Female arctiid moths, Utetheisa and insect sperm competition. Sperm Competition and the ornatrix, orient towards and join pheromonal choruses. Evolution of Animal Mating Systems (ed. by RL Smith), Animal Behaviour 75: 673–680. pp. 117–149. Academic Press, New York, NY, USA. 10 Gwynne & Lorch

Lorch PD (2002) Understanding reversals in the relative strength Shuker DM (2010) Sexual selection: endless forms or tangled of sexual selection on males and females: a role for sperm bank? Animal Behaviour 79: E11–E17. competition? American Naturalist 159: 645–657. Shuster SM (2011) Differences in relative fitness among alterna- Lorch PD (2005) Using upper limits of ‘Bateman gradients’ to tive mating tactics might be more apparent than real. Journal estimate the opportunity for sexual selection. Integrative and of Animal Ecology 80: 905–907. Comparative Biology 45: 924–930. Shuster SM & Wade MJ (2003) Mating Systems and Strategies. Lorch PD, Bussire L & Gwynne DT (2008) Quantifying the Princeton University Press, Princeton, NJ, USA. potential for using upper limits on Sutherland WJ (1987) Random and deterministic components of Bateman gradients. Behaviour 145: 1–24. variance in mating success. Sexual Selection: Testing the Alter- McCartney J, Kokko H, Heller K-G & Gwynne DT (2011) The natives (ed. by JW Bradbury & MB Andersson), pp. 209–219. evolution of sex differences in mate searching when females John Wiley & Sons, Chichester, UK. benefit: new theory and a comparative test. Proceedings of the Svensson BG (1997) Swarming behavior, sexual dimorphism, Royal Society of London B 279: 1225–1232. and female reproductive status in the sex role-reversed dance Parker GA & Simmons LW (1996) Parental investment and the fly species Rhamphomyia marginata. Journal of Insect Behavior control of sexual selection: predicting the direction of sexual 10: 783–804. competition. Proceedings of the Royal Society of London Thornhill R (1979) Male and female sexual selection and the evo- B 263: 315–321. lution of mating strategies in insects. Sexual Selection and Rhainds M (2010) Female mating failures in insects. Entomologia Reproductive Competition in Insects (ed. by M Blum & N Experimentalis et Applicata 136: 211–226. Blum), pp. 81–121. Academic Press, New York, NY, USA. Rhainds M, Gries G & Min MM (1999) Size- and density-depen- Thornhill R (1986) Relative parental contribution of the sexes to dent reproductive success of bagworms, Metisa plana.Entom- their offspring and the operation of sexual selection. Evolution ologia Experimentalis et Applicata 91: 375–383. of Animal Behavior: Paleontological and Field Approaches Robson LJ & Gwynne DT (2010) Measuring sexual selection on (ed. by MH Nitecki & JA Kitchell), pp. 113–135. Oxford Uni- females in sex-role-reversed Mormon crickets (Anabrus versity Press, New York, NY, USA. simplex, Orthoptera: Tettigoniidae). Journal of Evolutionary Vahed K (2003) Structure of spermatodoses in shield-back Biology 23: 1528–1537. bushcrickets (Tettigoniidae, ). Journal of Shields O (1967) Hilltopping: an ecological study of summit Morphology 257: 45–52. congregation behaviour of butterflies on a Southern Wheeler J, Gwynne DT & Bussie`re LF (2012) Stabilizing sexual California hill. Journal of Research on the Lepidoptera 6: selection for female ornaments in a dance fly. Journal of Evolu- 69–178. tionary Biology 25: 1233–1242.