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Keywords:

  • Allee effect;
  • bagworms;
  • emergence time;
  • empiricism;
  • flightlessness;
  • gynogeny;
  • paradigms in ecological theory;
  • parthenogenesis;
  • population density;
  • protandry;
  • Psychidae;
  • wallflower

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Definition of terms and scope of the review
  5. Methodological approaches to estimate female mating status
  6. A priori hypotheses derived from theoretical studies
  7. Incidence and causes of female mating failures across taxonomic orders
  8. Temporary vs. life-long wallflowers
  9. Conclusion
  10. Acknowledgements
  11. References

Empirical and experimental studies reporting the probability that some females remain unmated in field populations of insects (defined herein as mating failures) are reviewed in more than 100 species. The techniques used to quantify mating failures in the field are summarized, as well as factors that influence the probability that females mate during their lifetime. The existing empirical data provide partial support for hypotheses generated by theoretical models, although the trends observed in field populations are far more diverse and complex than predictions derived from ecological theory, e.g., the effect of population density on female mating success at small and large spatial scales is opposite. Mating success of females increases with the ratio of males in the population, but the relation between emergence time, sex ratio, and female mating success is variable. Females have evolved a broad range of physiological and behavioural adaptations to reduce mating failures, and exhibit a flexible context-dependent response to constraints limiting mating success. The large number of studies in Lepidoptera suggests a higher mating success in butterflies than moths. Examples of high rates of mating failure include species with gynogenous reproduction, long range migration, pre-reproductive maturation, male-biased sex ratio, acquisition of resources essential for reproduction, and female flightlessness. Species with sessile females that mate and oviposit near their emergence site provide model systems to investigate the causes and demographic consequences of female mating failure.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Definition of terms and scope of the review
  5. Methodological approaches to estimate female mating status
  6. A priori hypotheses derived from theoretical studies
  7. Incidence and causes of female mating failures across taxonomic orders
  8. Temporary vs. life-long wallflowers
  9. Conclusion
  10. Acknowledgements
  11. References

Most insect mating systems are characterized by larger reproductive investment by females than males, intense competition among males for access to females, and female discrimination between potential mates (Thornhill & Alcock, 1983). Although it is known that sexual activities often bear non-negligible costs for males (Wedell et al., 2002; Gwynne, 2008), fitness consequences of competitive interactions among females for access to males remain poorly understood (Rosenqvist & Berglund, 1992; Watson & Simmons, 2010). Mate choice by males has evolved under conditions where mating represents a significant investment for males (Bonduriansky, 2001). However, the causes and consequences of some females remaining unmated (defined herein as mating failure) in terms of sexual selection are not well understood (de Jong & Sabelis, 1991; Rhainds et al., 1995a; Kokko & Mappes, 2005).

In fact, the paradigm of near-complete female mating success pervades much of the entomological literature. Under this assumption, the fitness of females is strictly linked to fecundity and progeny survival [Reavey & Lawton, 1991; Cushman et al., 1994; but see Masters et al. (1994) and Fincke & Hadrys (2001)]. The lack of literature review on mating failure also hinders the conceptual development of competitive interactions among females for access to males. Even though many empirical studies document female mating failures in insect populations, the sources are eclectic and widely disseminated in the literature, and no consistent keyword is available for literature review. Similar concepts and approaches appear in studies of invasive species, release of biological control agents, evolution of mating systems, and mating disruption of pest species, but the absence of a consistent, well-defined conceptual terminology related to female mating failure has limited cross-talk among these fields of research.

This review consolidates field studies related to female mating failures in insects. The review is not exhaustive but includes more than 100 species for which field estimates of mating success are available (Tables 1–3), which makes it the most extensive thus far, not only for insects but also for any other group of animals or plants.

Table 1.   Insect species where high percentage of female mating success have been reported
Mating incidence (% mated)OrderFamilySpecies
50–75LepidopteraPapilionidaeParnassius clodius
PyralidaeChilo partellus
OrthopteraPyrgomophidaeSphenarium purpurascens
MecopteraPanorpidaePanorpa germanica
DipteraEmpilidaeRhamphomyia marginata
75–95OdonataCalopterygidaeLestes viridis
LepidopteraNoctuidaeHelicoverpa armigera, Helicoverpa punctigera, Spodoptera littoralis
PapilionidaeParnassius clodius, Parnassius smintheus, Parnassius phoebus, Papilio zelicaon
NymphalidaeCoenonympha pamphilus, Coenonympha tullia, Poladryas pola
HesperiidaeLerremus accius, Polites sabuleti
TortricidaeCydia pomonella
PieridaePieris protodice
HemipteraDelphacidaeDelphacodes scolochloa
>95LepidopteraPieridaeAporia crataegi, Pieris brassicae, Colias nastes, Pieris rapae, Pieris napi, Pontia daplidice, Anthocharis cardamines, Pieris protodice, Colias palaeno, Gonepteryx rhamni, Leptidea sinapsis, Colias philodice, Colias hyale, Colias eurytheme, Anthocaris sara
NymphalidaeChlosyne acastus, Euphydryas edita, Erebia ligea, Erebia pandrose, Maniola jurtina, Lopinga achine, Hipparchia semele, Aphantopus hyperantus, Coenonympha tullia, Lasiommata megera, Lasiommata maera, Inachis io, Hypolimnas bolina, Lasiommata petropolitana, Cercyonis pegala, Danaus gilippus, Speyeria cybele, Pararge aegeria, Polygonia c-album, Speyeria callipe semiviridae
PapilionidaePapilio zelicaon, Papilio philenor, Papilio glaucus, Papilio multicaudata, Battus philenor, Atrophaneura alcineus
PyralidaeAmyelois transitella
HesperiidaeAtalopedes campestris, Epargyreus clarus, Poanes viator, Hesperia sassacus, Polites mystic, Thymelicus lineola, Wallengrenia otho, Euphyes vestris
NoctuidaeEuxoa ochrogaster, Copitarsia consueta
ColeopteraDynastidaeOryctes monoceros
LampyridaePhotinus collustrans
OrthopteraAcrididaeChorthippus parallelus
TettigoniidaeMetrioptera roeseli
DipteraEmpididaeEmpis borealis
Table 2.   Insect species for which low incidence of mated females has been associated with a causal factor
Mating incidence (% mated)Order/family/speciesVariable
25–50LEPIDOPTERA
Geometridae, Alsophila pometariaGynogenous females (Harshman & Futuyma, 1985)
Papilionidae, Papilio zelicaonFemales captured at mating sites (hilltops) (Shields, 1967)
 Papilio eurymedon
 Anthocans athura
Pyralidae, Ostrinia nubilalisSamples in light traps for some time periods (Elliott, 1977)
Tortricidae, Cydia pomonellaLow section of host plants (Weissling & Knight, 1995)
Psychidae, Thyridopteryx ephemeraeformisHigh population density (Barrows, 1974)
 Low section of host plants (Rhainds & Sadof, 2009)
 Metisa planaSmall body size, high population density (Rhainds et al., 1999)
 Oiketicus kirbyiSmall body size, lower section of host plant, early emergence (Rhainds et al., 1995a,b)
Noctuidae, Heliothis virescensLate season (Proshold, 1991)
 Cnaphalocrocis medinalisEmergence time (Inoue et al., 2004)
COLEOPTERA
Scarabeidae, Oryctes monocerosSampled at oviposition sites (Allou et al., 2008)
ODONATA
Coenagrionidae, Ischnura graellsiiColour morphs, low population density (Cordero, 1992)
<25LEPIDOPTERA
Gelechiidae, Phthorimaea operculliLarge distance (360 m) from host plant (Cameron et al., 2005)
Lymantriidae, Lymantria disparLow population density, short distance (300 m) from area treated with mating disruptant (Sharov et al., 1995, 2002; Contarini et al., 2009)
Noctuidae, Mythimna separateMigrants without developed oocytes (Zhao et al., 2009)
 Euxoa ochrogasterYoung females (Gerber & Walkof, 1992)
Nymphalidae, Acraea encedonPopulations infected by male-killing bacteria (Jiggins et al., 2000; Jiggins, 2002)
 Acraea encedena
Pyralidae, Amyelois transitellaYoung females (Landolt & Curtis, 1991)
HEMIPTERA
Delphacidae, Ribautodelphax spec.Gynogenous females (den Bieman, 1988)
ARACHNIDAE
Araneidae, Nephila clavipesLate emergence (Higgins, 2000)
Table 3.   Insect species where variation in female mating success has been documented and related to a specific causal factor
SpeciesMethod1Factor2Reference
  1. 1FERT, fertility of eggs; ER, estimated encounter rate between males and females; SC, spermatophore counts; MR, mark–recapture studies; TF, tethered females; PMD, post-mortem dissection; PMF, post-mortem fecundity.

  2. 2BS, body size; ET, emergence time; SR, sex ratio; PD, population density; PHE, phenotype; AGE, age of female; HL, habitat location; MKB, male-killing bacteria; SITE, site.

ARACHNIDAE
 Misumena vatiaFERTBSLegrand & Morse, 2000
 Nephila clavipesERET, SRHiggins, 2000
HEMIPTERA
 Ribautodelphax spec.SCPDden Bieman, 1988
ODONATA
 Ischnura graellsiiMRPD, PHECordero, 1992
PHASMATOPTERA
 Tinema spec.SCPDSchwander et al., 2010
DIPTERA
 Rhamphomyia marginataSCAGESvensson, 1997
 Anopheles gambiaeSCSITECharlwood et al., 2003
 Contarinia sorghicolaERHLSharma & Vidyasagar, 1992
COLEOPTERA
 Oryctes monocerosSCAGE, HLAllou et al., 2008
ORTHOPTERA
 Chorthippus parallelusSCAGEReinhardt et al., 2007
 Requena verticalisSCETSimmons et al., 2007
 Sphenarium purpurascensMRSR, ET, BSdel Castillo & Núñez-Farfán, 2002
LEPIDOPTERA
Gelechiidae
 Phthorimaea operculellaTF, SCHLCameron et al., 2005
Lymantriidae
 Lymantria disparTF, ERPD, ETSharov et al., 1995; Robinet et al., 2007
Noctuidae
 Euxoa ochrogasterSCAGEGerber & Walkof, 1992
 Helicoverpa armigeraSCAGE, PDCoombs et al., 1993; Kehat et al., 1998
 Helicoverpa punctigeraSCAGECoombs et al., 1993
 Heliothis virescensSCETProshold, 1991
 Mythimna convectaSCETCoombs et al., 1993
Nymphalidae
 Acraea encedonSCMKBJiggins et al., 2000
 Melitaea cinxiaSCPD, AGEKuussaari et al., 1998
Oecophoridae
 Opisina arenosellaERETMuralimohan & Srinivasa, 2010
Papilionidae
 Papilio zelicaonSCAGE, HLShields, 1967; Sims, 1979
 Parnassius clodiusERETCalabrese et al., 2008
 Parnassius smintheusERETCalabrese et al., 2008
Pieridae
 Pieris protodiceSCPDShapiro, 1970
Psychidae
 Metisa planaPMDBS, PDRhainds et al., 1999
 Oiketicus kirbyiPMDSR, HLRhainds et al., 1995a,b
BS, ETRhainds & Cabrera-LaRosa, 2010
 Thyridopteryx ephemeraeformisPMDHL, PDBarrows, 1974; Rhainds et al., 2008; Rhainds & Sadof, 2009
Pyralidae
 Amyelois transitellaSCAGELandolt & Curtis, 1991
 Chilo partellusTF, SCPDUnnithan & Saxena, 1991
 Ostrinia nubilalisSCHLElliott, 1977
Tortricidae
 Cydia pomonellaTF, SCHLWeissling & Knight, 1995
 Choristoneura fumiferanaPMFAGEThomas et al., 1980
TF, SCPDKipp et al., 1995

Definition of terms and scope of the review

  1. Top of page
  2. Abstract
  3. Introduction
  4. Definition of terms and scope of the review
  5. Methodological approaches to estimate female mating status
  6. A priori hypotheses derived from theoretical studies
  7. Incidence and causes of female mating failures across taxonomic orders
  8. Temporary vs. life-long wallflowers
  9. Conclusion
  10. Acknowledgements
  11. References

Two trajectories may lead to females dying before they mate:

The article primarily reviews published reports of female mating failure defined as a dichotomous variable. Examples of pre-reproductive female death are included when they provide insight into mechanisms underlying mating failures. Some cage studies are reviewed but not tabulated as evidence of mating failures in field conditions, unless they were specifically designed to approximate natural conditions. Haplodiploid insects are not reviewed because fitness estimates of mating are difficult to measure (local mate competition, selection at the colony level, and non-zero fitness of unmated females) (Kranz et al., 2001; O’Donnell & Joyce, 2001) and comparative studies of virginity in this group are available (Hardy & Godfray, 1990; West et al., 1997). Arachnida are honorary guests of the review.

Methodological approaches to estimate female mating status

  1. Top of page
  2. Abstract
  3. Introduction
  4. Definition of terms and scope of the review
  5. Methodological approaches to estimate female mating status
  6. A priori hypotheses derived from theoretical studies
  7. Incidence and causes of female mating failures across taxonomic orders
  8. Temporary vs. life-long wallflowers
  9. Conclusion
  10. Acknowledgements
  11. References

Presence of a spermatophore

The presence or absence of a spermatophore with sperm in the reproductive tract of females can be used to determine their mating status (Stern & Smith, 1960). Assessing the presence of a spermatophore is by far the most common and practical approach to quantify female mating success, although interestingly the main purpose of this approach in most studies has been to document the incidence of multiple mating among field-collected females rather than the incidence of virgin females (Fischer, 2007; Kock & Sauer, 2008). The obvious drawback of the approach is its destructive nature (females have to be killed to assess the presence of spermatophore), thus it provides only a punctual snapshot of the mating status of females at one point in life. The problem can be partly overcome by simultaneously evaluating the presence of spermatophore and the age of females, based on wing wear or oocyte maturity (Sims, 1979; Landolt & Curtis, 1991; Gerber & Walkof, 1992; Coombs et al., 1993; Kuussaari et al., 1998), or recording the mating status of females repeatedly over time to account for the low mating success of predominantly young or immature females early in the season (Sims, 1979; Thomas et al., 1980; Baughman, 1991; Landolt & Curtis, 1991; Gerber & Walkof, 1992; Coombs et al., 1993; Svensson, 1997; Reinhardt et al., 2007; Simmons et al., 2007).

The presence or absence of a spermatophore among females sampled in a given population provides a useful estimate of the relative incidence of mating failure, as exemplified in two extreme scenarios: (1) The presence of a spermatophore in a vast majority (>95%; Table 1) of field collected females indicates a high level of mating success. (2) The absence of a spermatophore in many females, in contrast, likely reflects some mating failures, especially considering the potentially high mortality rate of virgin females (van Buskirk, 1987; Anholt, 1991; Widiarta et al., 1991; Tammaru et al., 2001; Tanhuanpää et al., 2003; de Block & Stoks, 2005). Simultaneous assessment of the daily rate of survival and mating status of female mosquitoes indicates that a large proportion of females fail to reproduce due to a lack of mating opportunity (Charlwood et al., 2003).

Presence of a mating plug

In some species, males deposit a conspicuous mating plug (sphragis) to prevent females from remating, thus allowing non-lethal field assessment (Matsumoto & Suzuki, 1992; Calabrese et al., 2008). A high proportion of females may subsequently lose the sphragis, however, which restricts the reliability of mating assessment (Orr, 2002; Vlasanek & Konvicka, 2009).

Presence of male-made mating marks

In some lepidopteran species, mating success can be inferred using the occurrence of male-made scale patches on the abdomen of females, although the reliability of this approach is variable; interestingly, the presence of patches on unmated females indicates unsuccessful mating attempts by males (Torres-Vila & McNeil, 2001).

Mark–recapture studies

Mark–recapture studies are useful to quantify pre-reproductive mortality (van Buskirk, 1987; Anholt, 1991) and the impact of emergence time or population density on female mating success (Cordero, 1992; Kindvall et al., 1998; del Castillo & Núñez-Farfán, 2002; de Block & Stoks, 2005). This approach can be applied only to large insects with a high recapture rate.

Tethered females

The use of tethered females has revealed significant predation before mating (Tammaru et al., 2001; Tanhuanpää et al., 2003) and restricted mating success at low population density (Sharov et al., 1995). This approach is prevalent in pheromone disruption trials, although mating communication may be disrupted in control plots beyond the area treated with pheromone (Sharov et al., 2002; Tcheslavskaia et al., 2005). Using tethered females precludes flight response from predators (Cooper, 2006; Almbro & Kullberg, 2008, 2009) and interferes with the foraging behaviour of mate-seeking females (Pearson et al., 2004). The later aspect is critical because mating success is sensitive to small variation (<1 m) in the vertical location of females (Sharma & Vidyasagar, 1992; Rhainds et al., 1995b; Weissling & Knight, 1995; Rhainds & Sadof, 2009).

Potential vs. realized fecundity

The positive relationship between body size and potential fecundity (Honek, 1993) can be used to estimate the number of eggs remaining in the bodies of dead females and the realized fecundity of females (Thomas et al., 1980; Rosenheim et al., 2008); by extension, the approach can also be used to assess the number of unmated females that did not lay eggs, assuming that failure to lay eggs is a reliable indicator of mating failure.

Dissection of post-reproductive females

Species with flightless females that mate and oviposit near their emergence site are amenable to a posteriori estimates of mating success. Bagworms (Lepidoptera: Psychidae), in particular, have frequently been investigated to identify causal factors related to female mating failure, using the presence or absence of eggs inside pupal cases of emerged females as a criterion for mating success (Rhainds et al., 2009).

A priori hypotheses derived from theoretical studies

  1. Top of page
  2. Abstract
  3. Introduction
  4. Definition of terms and scope of the review
  5. Methodological approaches to estimate female mating status
  6. A priori hypotheses derived from theoretical studies
  7. Incidence and causes of female mating failures across taxonomic orders
  8. Temporary vs. life-long wallflowers
  9. Conclusion
  10. Acknowledgements
  11. References

Theoretical studies have generated hypotheses relative to the extent, causes, and demographic consequences of female mating failure, but these models have often been developed in isolation from the empirical literature. In this section, specific predictions derived from theoretical models are summarized and contrasted with existing empirical data.

Population density and the Allee effect

Female mating failure has been conceptualized in ecological theory mainly from the angle of the Allee effect. Under this scenario, a large fraction of females in low density populations remain unfertilized, which may lead to a decline in per capita population growth rate (Allee, 1932; Andrewartha & Birch, 1954), extinction of local populations (Phillip, 1957; Cornell & Isham, 2004), interspecific competitive displacement (Scott, 1977), failure of establishment of biological control agents (Hopper & Roush, 1993), and restriction of geographic distributional range (Keitt et al., 2001).

Field studies conducted over a large spatial scale across multiple populations have revealed a positive relationship between population density and female mating success in three species, the Glanville fritillary (Kuussaari et al., 1998), the invasive gypsy moth (Contarini et al., 2009), and Tinema stick insects (Schwander et al., 2010). Additional support to the Allee effect is provided by unreplicated studies in three species, a pierid butterfly (Shapiro, 1970), a damselfly (Cordero, 1992) and the spruce budworm (Kipp et al., 1995). Reproductive failure among females at low population density has been hypothesized to restrict the establishment of hymenopteran parasitoids (Hopper & Roush, 1993), but unequivocal support of this hypothesis is lacking (Fauvergue et al., 2007).

Considering its limited empirical support, the mate encounter Allee effect should not be considered a principle of population ecology (Gascoigne et al., 2009), especially because several studies explicitly designed to detect its presence failed to do so (Kindvall et al., 1998; Fauvergue et al., 2007; Cronin, 2009; see also Kemp & Macedonia, 2007). The lack of support for the Allee effect is probably rooted in the difficulty in sampling low density popu-lation, but also in adaptations that counterbalance the effect of low male encounters [formation of leks or active female mate foraging in rare species (Shields, 1967; Scott, 1970, 1974), distinct flight and pheromone response of males at various densities (Cardé & Hagaman, 1984), strict selective pressures on efficient foraging by males (Legrand & Morse, 2000), selection of micro-habitat locations most attractive to males (Rhainds et al., 1995a), indiscriminate female mate choice at low population density (Kokko & Mappes, 2005) or when the rate of mate encounter is low (Shelly & Bailey, 1992)].

On a small scale, the mating success of females often declines with their relative abundance, which may be due to females interfering with each other in mate attraction (Barrows, 1974; Unnithan & Saxena, 1991; Kehat et al., 1998; Rhainds et al., 1999; see also Sharma & Vidyasagar, 1992). This counter-intuitive trend (in light of conventional wisdom regarding the Allee effect) suggests that population density has a variable effect on mating success depending on the spatial scale. Intense intraspecific competition resulting in small females at high population density may also yield an opposite prediction to that of the Allee effect (inverse density-dependent mating success), because small females are least attractive to males (Rhainds et al., 1995a, 1999; Svensson, 1997; Legrand & Morse, 2000; Cratsley & Lewis, 2005).

It is often overlooked that population density is not the only spatial parameter influencing female mating success. For example, the incidence of virgin females is considerably higher at lekking sites than other parts of the habitat (Shields, 1967). The mating success of females may or may not be affected by proximity to host plants (Kvedaras et al., 2000; Cameron et al., 2005) and tends to increase with their vertical position, an effect related to a more effective dissemination of pheromone from highest locations (Rhainds et al., 1995a,b; Weissling & Knight, 1995; Rhainds & Sadof, 2009). The response of mated and virgin females varies as a function of the source of host volatiles (Knight, 2006; Landolt & Guédot, 2008). In rhinoceros beetles, nearly all females captured in traps baited with male-produced sex pheromone are mated, compared with half of the females sampled at breeding sites where they oviposit (Allou et al., 2008). This contrasts with the Asian longhorn beetles where 100% of females captured in traps baited with male-pheromone or host plant volatiles alone are mated, compared with 15% of mated females in traps with a combination of pheromone and host volatiles (Nehme et al., 2010). The proportion of mated females may also vary as a function of their habitat: on average 4% of female corn borers sampled in the vegetation with a sweep net are virgin, compared with 23% of females captured at light traps (Elliott, 1977).

Emergence time, sex ratio, and reproductive asynchrony

The prevalence and adaptive significance of protandry (earlier emergence of males than females) has been the subject of a long-standing debate (Wiklund & Fagerström, 1977; Honek, 1997; Morbey & Ydenberg, 2001). One hypothesis holds that protandry is adaptive because it minimizes pre-reproductive death of females (Fagerström & Wiklund, 1982). Timing of emergence is expected to mediate female mating success through its effect on the operational sex ratio (Bessa-Gomes et al., 2004) and the degree of reproductive synchrony between males and females (Scott, 1977; Calabrese & Fagan, 2004). Theoretical models have estimated the mating success of females based on expected mate encounters, leading to the conclusions that (1) protandry enhances the mating success of both males and females under the assumptions that females mate once and encounter rates are high (Zonneveld & Metz, 1991), (2) most females mate during their lifetime under realistic field conditions (Botterweg, 1982; Wang et al., 1990) and (3) protandry restricts the mating success of late emergent females at low population density (Calabrese & Fagan, 2004; Robinet et al., 2007). However, mechanistic models based on passive mate encounters do not account for adaptations by which females increase mating success when access to males is limiting (Rhainds et al., 1995a; Wickman & Rutowski, 1999; Kokko & Mappes, 2005; Gowaty & Hubbell, 2009).

As predicted by theory, females emerging when and where males are most abundant tend to have a higher mating success (Rhainds et al., 1995b; Higgins, 2000; del Castillo & Núñez-Farfán, 2002; Muralimohan & Srinivasa, 2010; Rhainds & Cabrera-LaRosa, 2010), although a broad range of patterns have been documented with regards to the relation between emergence time and female mating success. Late emerging females have a low mating success in protandrous populations due to a shortage of males (Higgins, 2000; Calabrese et al., 2008; Muralimohan & Srinivasa, 2010) (Figure 1A). In other species, females emerging during the middle portion of the emergence cycle have a higher mating success, which corresponds to the time period where the proportion of males is at its peak level (del Castillo & Núñez-Farfán, 2002) (Figure 1B). The optimal timing of female emergence may reflect a trade-off between minimizing pre-reproductive death and achieving a large size as adult (Kleckner et al., 1995).

image

Figure 1.  Mating success of females in relationship with the emergence time of adults. (A) Low mating success of late emerging females in protandrous Opisina arenosella Walker (Lepidoptera: Oecophorida): the presence or absence of larval progeny in surrounding host plants was used to determine whether or not females emerging during different time periods mated; the low mating success of late emerging females coincided with a low ratio of males per female (Muralimohan & Srinivasa, 2010). (B) High mating success of female Sphenarium purpurascens Charpentier (Orthoptera: Pyrgomorphidae) emerging in mid-season, when the sex ratio is most male-biased; mating status was recorded using an intensive mark–recapture study (del Castillo & Núñez-Farfán, 2002). (C) Low mating success of late emerging females in migratory Heliothis virescens Fabricius (Lepidoptera: Noctuidae); variation in mating success was likely due to the high incidence of obligatory mating events late in the season. The mating status of females was determined using the presence or absence of a spermatophore (Proshold, 1991). (D) Low mating success of early emerging females in the protogynous bagworm Oiketicus kirbyi Guilding (Lepidoptera: Psychidae); the mating status of females was evaluated using post-mortem dissection of female bags (Rhainds et al., 1995b). (E) Random temporal variation in mating success of female Ostrinia nubilalis Hübner (Lepidoptera: Pyralidae); insects were sampled using light traps, and the mating success of females determined using as a criterion the presence or absence of a spermatophore (Elliott, 1977).

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In the Noctuidae, a taxonomic group characterized by obligatory migrations, the apparently low mating success of late emerging females is likely not related to variation in sex ratio but rather to temporal patterns of migration events (Figure 1C; Proshold, 1991; Gerber & Walkof, 1992; Coombs et al., 1993; Torres-Vila & McNeil, 2001; Inoue et al., 2004). The process of migration typically involves long-range dispersal by sexually immature females, followed by ovarian development and mating at the end of the migration (Zhao et al., 2009). The high proportion of mated females among individuals with mature oocytes suggests that migrant females usually mate (Gerber & Walkof, 1992; Coombs et al., 1993), but mortality during dispersal bouts is difficult to evaluate (Ward et al., 1998).

Although protandry is prevalent in insects, protogyny (earlier emergence of females than males) is more common than usually thought (Honek, 1997). In reproductively isolated bagworm populations (discrete generations, synchronous development across a large spatial scale), protogyny is associated with mating failures among early emerging females (Rhainds et al., 1995b) (Figure 1D). The adaptive significance of protogyny in bagworms is unclear, because strong selective pressures are expected to synchronize the emergence of males and females due to the low mating success of early emerging females and late emerging males. In some species, variation in mating success is independent of emergence time or local sex ratio (Figure 1E; Elliott, 1977; Sadek, 2001), which may be attributed to effective male dispersal inter-connecting local populations (Rhainds et al., 2008).

Late emergence of small, least fecund females, at a time when males have few mating opportunities (Carvalho et al., 1998), may represent an example of the wallflower paradox where the composition of sexually active females changes during the course of the season (increasing share of females with traits less preferred by males), thus increasing the probability of small females to mate (de Jong & Sabelis, 1991).

Female adaptations to reduce the incidence of mating failure

Random mating encounters and low female mating success, particularly in sparse populations, have been hypothesized to lead to the evolution of adaptations enhancing mating success (Mosimann, 1958; Fauvergue et al., 1995; South & Kenward, 2001; Jonsson et al., 2003; Pearson et al., 2004). Females have indeed evolved extravagant physiological adaptations (Funk & Tallamy, 2000; Arnqvist et al., 2007; Kaufman, 2007) and a set of behaviours to increase their probability of mating, ranging from active foraging for mates (Wickman, 1986; Kaitala & Wiklund, 1994; Mendoza-Cuenca & Maćias-Ordóñez, 2009), aggressive interactions among conspecifics for access to males (Lynam et al., 1992; Papadopoulos et al., 2009), and selection of habitats most suitable for mate attraction (Shields, 1967; Scott, 1970; Rhainds et al., 1995a,b; Rhainds & Sadof, 2009). Females have further evolved covert behavioural adaptations to ensure that they mate at least once, e.g., indiscriminate mate choice of virgin females compared with mated females (Svensson et al., 1998; Kokko & Mappes, 2005; Peretti & Carrera, 2005; Kumano et al., 2009).

From a female perspective, the costs of sexual reproduction include metabolic expenditure associated with a delay in reproduction (Wing, 1989; Jones et al., 2008; Barrett et al., 2009), predation risk (Wing, 1988; Almbro & Kullberg, 2009), energetic investment associated with mate foraging (Wickman & Jansson, 1997), interference with acquisition of resources essential for reproduction (Kaufman, 2007), and the risk of mating failure. The mating strategy of females often reflects a trade-off between reducing the probability of mating failure and minimizing other mating costs. For example, in populations with extreme-female biased sex ratio and depressed mating success, females have evolved sex-role reversal and aggregate at landmarks to solicitate mating from males (Jiggins et al., 2000; Jiggins, 2002). Females adopt different foraging strategies depending on their emergence time and the relative availability of males (Mendoza-Cuenca & Maćias-Ordóñez, 2009), or exhibit a low degree of mate choosiness when the reproductive season is short (Friberg & Wiklund, 2007), the rate of mate encounter low (Gotthard et al., 1999; Cratsley & Lewis, 2005; Kokko & Rankin, 2006), and life span brief (Wickman, 1992). Females adjust their mate signalling as they age (Wing, 1991) or in response to the presence of competing females (Lim & Greenfield, 2006).

The evidence for a strict evolutionary linkage between adaptations to reduce mating failure and constraints related to low population density is tenuous. Females that fail to mate have zero fitness and do not contribute to the genetic pool in the next generation. Stringent selective pressures are thus expected to favour adaptations that enhance female mating success across a broad range of ecological context where mating failure arises. The response of females to constraints limiting mating success is flexible and condition-dependent, thus it seems unlikely that these adaptations have evolved strictly to enhance mate encounter rates in sparse populations.

Female flightlessness and constrained mating success

It has been hypothesized that flightlessness of females per se constrains the mating success of females (Bell, 1982; Roff, 1990; Denno, 1994). Indirect support for this hypothesis is provided in a wing-dimorphic insect whose wingless females (but not winged females) produce a dorsal secretion (nuptial gift) to attract and retain males for mating (Arnqvist et al., 2007), and also by the high incidence of mating failures in species with flightless females (Harshman & Futuyma, 1985; Sharov et al., 1995; Rhainds et al., 2009). Female flightlessness may have a particularly severe depressing effect on mating success when species exploit ephemeral or structurally complex habitats (Denno, 1994). Intense natural selection on efficient mate foraging by males, however, may result in near complete female mating success in species with sedentary females, even when the population is low and the sex ratio female-biased (Wing, 1984; Legrand & Morse, 2000). To date, only one field study has evaluated the mating success of different female morphs in species with wing dimorphism, and reported no difference in the proportion of mated females among brachypters and macropters, either in established populations or recently colonized environments (Cronin, 2009).

Parthenogenetic reproduction is expected to have evolved in taxonomic groups with high rate of mating failure (Gerritsen, 1980). Parthenogenesis has been reported in many insect taxa, especially those with a high incidence of flightless females (Bell, 1982; Roff, 1990; Rhainds et al., 2009), and the hypothesis that low mating success of flightless females favours the evolution of parthenogenesis was recently supported in Tinema stick insects (Schwander et al., 2010).

Taxonomic groups with both flighted and flightless females (in particular Curculionidae, Geometridae and Lymantriidae) represent ideal systems to test for the effect of female mobility on mating success. Unfortunately, data are available for only one lymantriid, the gypsy moth (Contarini et al., 2009), and one geometrid, the fall cankerworm, a species with flightless females and gynogenous reproduction (Harshman & Futuyma, 1985). Gynogeny (or sperm-dependent parthenogenesis) represents an unusual mode of reproduction in which females need to mate before reproducing, but the male makes no genetic contribution to the offspring (Beukeboom & Vrijenhoek, 1998; Schlupp, 2005). Gynogenous females coexist with a closely related sexual (male-producing) species to reproduce, compete with sexual females for access to males, and have a reproductive advantage over sexual females because they do not bear the cost of producing males, theoretically leading to an ever increasing ratio biased toward gynogenous females, up to the point where the population goes extinct due to a lack of males. Limited availability of sperm results in a high proportion of female mating failures in gynogenous females (Harshman & Futuyma, 1985; Kirkendall, 1990), however, especially because males preferentially mate with sexual females over gynogenous females (den Bieman, 1988; Loyning & Kirkendall, 1996; Schlupp, 2005). The proportion of mated gynogenous females increases with the ratio of sexual female per gynogenous female, i.e., as the proportion of males in the population increases (den Bieman, 1988; Loyning & Kirkendall, 1996; Schlupp, 2005). Gynogeny has evolved several times independently in insects, both in taxa with flighted or flightless females (Beukeboom & Vrijenhoek, 1998; Schlupp, 2005), thus it provides a model system to evaluate ecological and evolutionary constraints associated with female flightlessness and mating success.

Pre-reproductive dispersal of adults has evolved to reduce the potentially high fitness cost of inbreeding (Motro, 1991; Gandon, 1999; Lehman & Perrin, 2003; Hirota, 2004). In many species, however, adults do not disperse from their natal patch and mate among siblings (Masters et al., 1994; Avilés & Gelsey, 1998; Bilde et al., 2005; de Luca & Cocroft, 2008). Females in these resident mating aggregations adjust the sex ratio of their progeny to reduce local mate competition (Sabelis & Nagelkerke, 1988; Masters et al., 1994; Nagelkerke & Sabelis, 1998; West et al., 2005). The evolutionary transition between mating systems characterized by pre-reproductive adult dispersal or resident inbred mating (Avilés & Gelsey, 1998; Bilde et al., 2005; Agnarsson et al., 2006) possibly illustrates the cost of adult dispersal in terms of female mating failure.

Incidence and causes of female mating failures across taxonomic orders

  1. Top of page
  2. Abstract
  3. Introduction
  4. Definition of terms and scope of the review
  5. Methodological approaches to estimate female mating status
  6. A priori hypotheses derived from theoretical studies
  7. Incidence and causes of female mating failures across taxonomic orders
  8. Temporary vs. life-long wallflowers
  9. Conclusion
  10. Acknowledgements
  11. References

Empirical data relative to female mating failure have been published in two ararchnid species and nine orders of insects (Tables 1–3). Studies in the Lepidoptera (n = 88 species) far outnumber those in other orders (Orthoptera: 4; Diptera: 4; Coleoptera: 2; Thripidae: 2; Hemiptera: 2; Mecoptera: 1; Odonata: 1; Phasmatoptera: 1). Mating success is usually high in butterflies, with more than 75% (usually 95%) of mated females in most species (Table 1). In moth species, in contrast, both high and low mating success have been reported (Tables 1 and 2). Extreme variation of mating success has been reported in the Noctuidae (Torres-Vila & McNeil, 2001), but this is most likely due to captures of young, virgin females with undeveloped oocytes (Tables 1 and 2). Interestingly, extreme variation in the ratio of virgin females has been reported in two species of dance flies with otherwise similar mating system (Svensson, 1997). Levels of high and low mating success have been documented in the Coleoptera and Hemiptera, but sample size in terms of species is too low to draw conclusions. Low mating success of females appears common in bagworms (Table 2), which may be due to the sessile nature of the females.

Across taxonomic orders, low mating success (<50% of mated females) is associated with a low position on the host plant (three species), early or late emergence time (three species), low or high population density (four species), and gynogenous reproduction (two species) (Table 3). Phenotypic variation in body size has an effect on mating success in some species, with large females most likely to mate (Tables 2 and 3). The proportion of mated females commonly fluctuates as a function of age (Tables 2 and 3), but the low mating success of young females represents a transient stage in the life of females that may mate as they grow older. Spatial variables that influence mating success include habitat location (eight species) or popu-lation density (10 species, excluding studies where no effect of population density was detected) (Table 3). Temporal variation in emergence time influence female mating success in 10 species (Table 3).

Temporary vs. life-long wallflowers

  1. Top of page
  2. Abstract
  3. Introduction
  4. Definition of terms and scope of the review
  5. Methodological approaches to estimate female mating status
  6. A priori hypotheses derived from theoretical studies
  7. Incidence and causes of female mating failures across taxonomic orders
  8. Temporary vs. life-long wallflowers
  9. Conclusion
  10. Acknowledgements
  11. References

The probability of mating failures has been conceptualized as a wallflower effect in which females least preferred by males become numerically more abundant over time, thus increasing their probability of mating (de Jong & Sabelis, 1991). Under this scenario (temporary wallflowers), no runaway sexual selection of female traits is expected because all females eventually mate during their lifetime, although a long interval between sexual maturity and mating may reduce the fitness of females. Species that exhibit a high (>95%, Table 1) percentage of mated females exemplify mating systems with limited wallflower effects. In other species, the apparently high rate of mating failure may represent temporary wallflowers, e.g., females without a spermatophore at the time of sampling may have eventually mated during the remaining portion of their life (Table 3). The use of tethered females or of females sampled at different locations helps to identify ecological parameters that influence mating success, but results obtained using these techniques cannot be directly converted in temporary or life-long wallflowers due to the experimental nature of the data.

In many insect species, a significant proportion of unmated females die as virgin (life-long wallflowers). Considering the potentially high rate of mortality among adults, for example, populations characterized by a high proportion of females without a spermatophore (Tables 2 and 3) likely exhibit life-long wallflowers. The recurrence of female mating failures across taxonomic orders poses a challenge to evolutionary theory, because life history traits associated with mating failure would be expected to be rare or even absent. Examples of seemingly extreme rate of female mating failure (up to 50%) include species with gynogenous reproduction, long range migration, pre-reproductive maturation, male-biased sex ratio, acquisition of resources essential for reproduction, and female flightlessness (Table 2).

Conclusion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Definition of terms and scope of the review
  5. Methodological approaches to estimate female mating status
  6. A priori hypotheses derived from theoretical studies
  7. Incidence and causes of female mating failures across taxonomic orders
  8. Temporary vs. life-long wallflowers
  9. Conclusion
  10. Acknowledgements
  11. References

This review consolidates the literature on female mating failures and competitive interactions among females for access to males in populations of insects. The major trends identified in the literature highlight critical research areas for future studies.

Field estimates of female mating status rely mostly on the presence or absence of a spermatophore in the genitalia. This approach provides relative estimates of either temporary or life-long wallflowers, depending upon the probability that females mate in the remainder of their hypothetical (post-sampling) life. Studies that simultaneously evaluate the daily rate of adult survival and mating probability are few and particularly welcome.

The large number of studies in Lepidoptera provide source material to derive at the intraspecific level causal factors linked with variation in mating probability, and to develop at the interspecific level a meta-analysis on life history traits associated with mating failure, e.g., higher mating success in butterflies than moths, evolutionary association between female flightlessness, mating failure and parthenogenetic reproduction.

The mating success of females increases with the proportion of males in the population and is affected by other parameters such as population density, habitat location, and emergence time, although the effect of these factors is variable. A meticulous blend of empiricism and theory is needed to generate a priori hypotheses that can be experimentally tested for different mating systems.

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  1. Top of page
  2. Abstract
  3. Introduction
  4. Definition of terms and scope of the review
  5. Methodological approaches to estimate female mating status
  6. A priori hypotheses derived from theoretical studies
  7. Incidence and causes of female mating failures across taxonomic orders
  8. Temporary vs. life-long wallflowers
  9. Conclusion
  10. Acknowledgements
  11. References
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