Why are female color polymorphisms rare in territorial damselflies?

In nonterritorial damselflies, females often come in multiple color morphs, perhaps because females with rare colors experience reduced sexual harassment, and thus have a frequency‐dependent fitness advantage, compared to females of the most common color morph, but such polymorphisms are rare in territorial species. We consider three hypotheses to explain the rarity of female color polymorphisms in territorial species: (a) misdirected male aggression, (b) poor male mate recognition, and (c) low mating harassment rates. The first hypothesis has some empirical support, and can account for the absence of andromorphs (i.e., females that resemble males), but does not explain the absence of multiple heteromorphs. We tested the second hypothesis by presenting females of two novel color morphs (green‐ or red‐banded abdomens) to territorial male Hetaerina capitalis. Females of both novel color morphs elicited fewer sexual responses than control females, and the red morph occasionally elicited aggressive responses. These results indicate that novel female color morphs would experience reduced mating harassment in this species, contradicting the hypothesis that male mate recognition is too poorly developed to reduce harassment of novel female morphs. By process of elimination, the third hypothesis, that harassment rates are too low in territorial species to provide rare female morphs a fitness advantage, is favored, but remains untested. Our findings also suggest that the common practice of color‐marking odonates for behavioral research is likely to interfere with mate choice, as has long been known to be the case in birds.     

Male disguised females: costs and benefits of female‐limited dimorphism in a butterfly

1. In polymorphic species, two or more discrete phenotypes co‐occur simultaneously. Sex‐limited polymorphism is a particular case of polymorphism, in which several discrete morphs coexist within one of the two sexes only. Several hypotheses were proposed to explain the existence and the maintenance of sex‐limited polymorphism in insects: (i) the morphs have similar fitness, such as similar survival and expected fecundity, and their frequencies vary randomly (i.e. the null hypothesis); (ii) harassment by males is reduced towards the less common female morph, in this case andromorph females (i.e. the male mimicry and learned mate recognition hypotheses); (iii) morphs differ in predation risk (i.e. the predation hypothesis); or (iv) morphs differ in thermoregulation ability (i.e. the thermoregulation hypothesis). 2. Field observations and experiments were employed to compare the relative support of these hypotheses using dimorphic females of the bog fritillary butterfly. Differences were detected between morphs in survival, fecundity, harassment by males, predation pressure and thermal properties, thereby rejecting the null hypothesis. 3. The lifestyle of both morphs is associated with different costs and benefits, with advantages in daily survival and precocious emergence for the gynomorph females, and advantages in fecundity, predation and male harassment for the andromorph females. Besides, as the bog fritillary butterfly is protandrous (i.e. males emerge before females), the longer development of andromorph females puts them at risk of emerging when all the males are dead. The results raise the question as to which mechanisms control the ontogenetic pathways driving the production of the two morphs (i.e. genetic polymorphism or phenotypic plasticity).     

Testing the role of coadapted genes versus bet-hedging for mating strategies in colour polymorphic pygmy grasshoppers

Recent investigations of mate choice indicate that the genetic effect of sires on offspring fitness may depend on the interaction between maternal and paternal genotypes and the environmental conditions experienced by the offspring. Alternative colour morphs of the pygmy grasshopper, Tetrix subulata , represent ecological strategies that differ in body size, life history, thermoregulatory behaviour, and habitat selection. The hypothesis that selection promotes behaviours maintaining coadapted gene complexes predicts individuals to mate assortatively with respect to colour morph. On the other hand, the bet-hedging hypothesis predicts that the temporal variability of the environment inhabited by these animals may select for disassortative mating behaviour resulting in heterogeneous offspring. To distinguish between these competing hypotheses, we investigated mating behaviours using dual-choice experiments. Our results were not in agreement with the prediction of assortative mating but suggest instead that matings were random with regard to colour morph. Polyandry was common, and females mated with the second male regardless of whether the first mating was assortative or disassortative. Polyandry also was equally frequent among females in triads in which the two males belonged to different colour morphs as in triads where both males belonged to the same colour morph. A field experiment confirmed that polyandry occurred also among free-ranging individuals, and uncovered variation in mating success among male colour morphs, probably due to indirect effects of coloration on activity or habitat use. The consequences of this random and polyandrous mating strategy for the evolutionary dynamics of the colour polymorphism remain to be explored.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 491–499.     

Common Wall Lizard Females (Podarcis muralis) do not Actively Choose Males Based on their Colour Morph

Identifying the processes that lead to the evolution and maintenance of links between colour morphs and behavioural strategies has implications for the evolution of reproductive isolation and sympatric speciation. Sexual selection may play a significant role in the evolution of colour pattern complexity in reptiles, particularly when there are fitness consequences associated with mating with males of different colour morphs. In this article, we explored if common wall lizard females (Podarcis muralis) actively select males according to their morph in a colour‐assortative pattern using a multiple‐choice experiment with both visual and chemical cues. We failed to identify female active mate choice, as females did not choose males based on male colouration or femoral pore secretions. Indeed, females equally entered the three preference compartments and spent nearly the same amount of time within them, irrespective of both colour and odour of males. Consequently, our results do not support the hypothesis that colour polymorphism in this species may be driven by colour‐assortative mating promoted by females. However, we cannot exclude the possibility that females may choose males according to their colour following a flexible choice strategy, nor the possibility that females actively discriminate among males according to qualities that are not directly related to morph‐specific strategies.     

Temperature drives pre‐reproductive selection and shapes the biogeography of a female polymorphism

Conflicts of interests between males and females over reproduction is a universal feature of sexually reproducing organisms and has driven the evolution of intersexual mimicry, mating behaviours and reproductive polymorphisms. Here, we show how temperature drives pre‐reproductive selection in a female colour polymorphic insect that is subject to strong sexual conflict. These species have three female colour morphs, one of which is a male mimic. This polymorphism is maintained by frequency‐dependent sexual conflict caused by male mating harassment. The frequency of female morphs varies geographically, with higher frequency of the male mimic at higher latitudes. We show that differential temperature sensitivity of the female morphs and faster sexual maturation of the male mimic increases the frequency of this morph in the north. These results suggest that sexual conflict during the adult stage is shaped by abiotic factors and frequency‐independent pre‐reproductive selection that operate earlier during ontogeny of these female morphs.     

Preference for Male Traits Differ in Two Female Morphs of the Tree Lizard,Urosaurus ornatus

Non-random female mating preferences may contribute to the maintenance of phenotypic variation in color polymorphic species. However, the effect of female preference depends on the types of male traits used as signals by receptive females. If preference signals derive from discrete male traits (i.e., morph-specific), female preferences may rapidly fix to a morph. However, female preference signals may also include condition-dependent male traits. In this scenario, female preference may differ depending on the social context (i.e., male morph availability). Male tree lizards (Urosaurus ornatus) exhibit a dewlap color polymorphism that covaries with mating behavior. Blue morph males are aggressive and defend territories, yellow males are less aggressive and defend smaller territories, and orange males are typically nomadic. Female U. ornatus are also polymorphic in dewlap color, but the covariation between dewlap color and female behavior is unknown. We performed an experiment to determine how female mate choice depends on the visual and chemical signals produced by males. We also tested whether female morphs differ in their preferences for these signals. Female preferences involved both male dewlap color and size of the ventral color patch. However, the female morphs responded to these signals differently and depended on the choice between the types of male morphs. Our experiment revealed that females may be capable of distinguishing among the male morphs using chemical signals alone. Yellow females exhibit preferences based on both chemical and visual signals, which may be a strategy to avoid ultra-dominant males. In contrast, orange females may prefer dominant males. We conclude that female U. ornatus morphs differ in mating behavior. Our findings also provide evidence for a chemical polymorphism among male lizards in femoral pore secretions.     

Male mate choice and the potential for complex mating dynamics in the tree lizard (Urosaurus ornatus)

A growing body of literature is recognizing that males may also play a role in the mating process by behaving non‐randomly toward potential female mates during courtship. In numerous species, discrete color polymorphisms in males are inferred to represent alternative mating tactics, which often correspond with concomitant asymmetries in ecology and behavior. In terms of their mating behavior, these ecological outcomes of a color polymorphism should affect a morph's likelihood and frequency of encountering females in a population, possibly favoring the evolution of morph‐specific mating preferences. Knowledge of how male morphs contribute to a species’ overall mating dynamics will improve our understanding of how sexual selection shapes phenotypic diversity in color polymorphic systems. We conducted a mate choice experiment to evaluate the extent and morph specificity of non‐random mating preferences by male ornate tree lizards, Urosaurus ornatus. We observed the behavior of blue and yellow males in an experimental arena in response to a choice between an orange or yellow female. We found that blue males preferred yellow females over orange females, and although yellow males visited females more often than blue males overall, their attention was not morph‐specific. Given male morph differences in choosiness, and their differences in social dominance, we conclude that female throat color may be partly under sexual selection in U. ornatus. However, a lack of concordance between male and female mating preferences (drawn from an earlier study) suggests that overall mating dynamics may serve to maintain, rather than enhance, color morph differences in this species.     

Variety is the Spice of Life: Female Lizards Choose to Associate with Colour-Polymorphic Male Dyads

We test the idea that male colour polymorphism in a lizard (red vs. yellow headed) may be maintained by a female preference for associating (and presumably mating) with both male morphs rather than only one. In female choice experiments on single males of different colours, females did not preferentially associate with either morph. However, when females were allowed to choose between pairs of males of the same vs. different colours, they preferred to associate with male pairs that were polymorphic. We suggest that this may be the result of selection arising from polyandrous mating benefits and show experimentally that polyandry results in increased hatching success. Most theoretical models of the evolution of mate choice assume that mate choice is costly. We test this assumption by releasing females into polymorphic vs. monomorphic groups in the wild, under the hypothesis that females move more between males in polymorphic groups and therefore suffer higher risks of mortality from predation. In accordance with this prediction, females released into polymorphic male groups were less likely to be recaptured than females released into monomorphic groups, with evidence to suggest that this is because of increased mortality and not increased dispersal. We propose that this cost could be (partly) balanced by polyandrous fitness benefits.     

Differences in Mating Propensity Between Immature Female Color Morphs in the Damselfly Ischnura elegans (Insecta: Odonata)

Female-limited color polymorphisms occur in a variety of animal taxa where excessive male sexual harassment may explain the coexistence of multiple female color morphs. In the color polymorphic damselfly Ischnura elegans, mature and immature female color morphs coexist at the mating site where males are in search for suitable mating partners. Here, we study male preference and female mating propensity for the two immature female morphs. As would be expected, compared to mature morphs, both immature female morphs mate much less. Within immature females, one morph consistently mates more frequently compared to the other morph, a pattern that is similar for the ontogenetically corresponding mature female morphs. Preference experiments with the two differently colored immature female morphs, however, did not indicate male mate preference for either morph. Low mating frequencies of immature females at natural sites in combination with relatively high attractiveness of immature models in terms of male preference indicate that female behavior influences female mating success.     

Colour Polymorphism and Alternative Breeding Strategies: Effects of Parent’s Colour Morph on Fitness Traits in the Common Wall Lizard

Colour polymorphism (CP) is widespread in animals, but mechanisms underlying morph evolution and maintenance are not completely resolved. In reptiles, CP is often genetically based and associated with alternative behavioural strategies, mainly in males for most cases. However, female colour morphs also display alternative reproductive strategies associated with behavioural and physiological traits, which may contribute to maintain CP in the population. Both sexes of the common wall lizard (Podarcis muralis) show three pure colour morphs, white, yellow and red. Here, we looked for the effects of male and female colour morphs on fitness traits of captive-breeding pairs. All yellow-throated females laid clutches of many small eggs and produced many light offspring, behaving as r-strategists, whereas white-throated females laid clutches of few large eggs and produced few heavy offspring, behaving as K-strategists. Red-throated females adopted a conditional Kr-strategy depending on their size/age. These basic female strategies were modulated in relation to mate morph: white females had the best fitness gain in terms of viable offspring when mated to red males; mating between yellow morphs yielded a greater breeding success than all other morph crosses, but also lighter offspring; finally, red females produced heavy progeny when paired with red or white males, and light offspring in pair with yellow males. Thus, correlation between CP and traits relevant to fitness combined with non-random mating, either assortative or disassortative, could increase the potential for CP to contribute to divergent evolution in the common wall lizard.     

Intrasexual mounting in the beetle Diaprepes abbreviatus (L.).

The weevil Diaprepes abbreviatus shows three kinds of same-sex mountings: males mount other unpaired males, males mount males already engaged in copulation and females mount other females. Four hypotheses were evaluated in order to explain same-sex matings by males: (i) female mimicry by inferior males, (ii) dominance of larger males which affects the behaviour of small males, (iii) sperm transfer in which smaller males gain some reproductive success by 'hitchhiking' their sperm with the sperm of larger males, and (iv) poor sex recognition. Data from mate choice and sperm competition experiments rejected the female mimicry, dominance and sperm transfer hypotheses and supported the poor sex recognition hypothesis. We tested three hypotheses in order to explain female mounting behaviour: (i) females mimic male behaviour in order to reduce sexual harassment by males, (ii) females mount other females in order to appear larger and thereby attract more and larger males for mating, and (iii) female mimicry of males. The results of our mate choice experiments suggested that the female mimicry of males hypothesis best explains the observed female mounting behaviour. This result is also consistent with the poor sex recognition hypothesis which is the most likely explanation for male and female intrasexual mating behaviour in many insect species.     

Reflectance spectra and mating patterns support intraspecific mimicry in the colour polymorphic damselfly <Emphasis Type="Italic">Ischnura elegans</Emphasis>

Coexistence of female colour morphs in animal populations is often considered the result of sexual conflict, where polymorphic females benefit from reduced male sexual harassment. Mate-searching males easily detect suitable partners when only one type of female is present, but become challenged when multiple female morphs coexist, which may result in frequency-dependent mate preferences. Intriguingly, in damselflies, one female morph often closely resembles the conspecific male in body coloration, which has lead to hypotheses regarding intra-specific male-mimicry. However, few studies have quantitatively evaluated the correspondence between colour reflectance spectra from males and male-like females, relying instead on qualitative visual assessments of coloration. Using colour analyses of reflectance spectra, we compared characteristics of the body coloration of ontogenetic male and female colour morphs of the damselfly Ischnura elegans. In addition, we evaluated whether males appear to (1) discriminate between immature and mature female colour morphs, and (2) whether male-like females experience reduced male mating attention and low mating frequencies as predicted from male-mimicry. Spectral reflectance data show that immature female morphs differ substantially in coloration from mature individuals. Mating frequencies were much lower for immature than mature female morphs. For the male-like female morph, measures of colour were statistically indistinguishable from that of both immature and mature conspecific males. Mating frequencies of male-like females were lower than those of other mature female morphs under field and experimental conditions. Together, our results indicate that males may use the observed spectral differences in mate choice decisions. Furthermore, male-like females may be regarded as functional mimics that have reduced attractiveness and lowered rates of sexual harassment by mate-searching males.     

Evolution of female colour polymorphism in damselflies: testing the hypotheses

The existence of several female colour morphs is a conspicuous characteristic of many damselflies that show one male-like (androchrome) and several nonmale-like (gynochrome) morphs. We tested several adaptive hypotheses and the null model for the maintenance of female polychromatism (one androchrome and two gynochromes) in the damselfly Ceriagrion tenellum. We tested the null model by comparing the degree of genetic differentiation between the colour locus and a set of 19 neutral RAPD loci in five populations. Our results indicate that selection is acting to maintain similar frequencies between populations at the colour locus. Using mark–recapture techniques we found that mating success is not dependent on female coloration. We tested the mimicry hypothesis by presenting live and dead models to males. Dead models were highly attractive irrespective of coloration. In contrast, with live models males could not distinguish between androchromes and other males, and were more attracted to gynochrome females. Despite this, within populations morph frequencies remained constant over time and mating was at random with respect to female coloration. However, there was a positive relationship between male density and androchrome frequency in a comparative study of eight populations. We discuss our results in the framework of sexual conflict theory and suggest that andro- and gynochrome females are using different strategies to control their number of matings. The different morphs might be maintained in a balanced polymorphism by a combination of density- and frequency-dependent mechanisms.Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour     

Female ground tits prefer relatives as extra‐pair partners: driven by kin‐selection?

Socially monogamous female birds routinely mate with males outside the pair bond. Three alternative hypotheses consider genetic benefits as the major driver behind the female strategy. The inbreeding avoidance hypothesis predicts that females paired with closely related males should seek copulations with distantly related extra-pair partners to avoid fitness loss from inbreeding depression; the outbreeding avoidance hypothesis predicts the opposite; the kin-selection hypothesis suggests that regardless of social mate relatedness, females should give related males extra-pair fertilization opportunities to gain inclusive fitness if the costs from inbreeding are minor. We test these hypotheses with a facultative cooperative breeder, the ground tit (Parus humilis). Social pairs of ground tits formed randomly with respect to genetic relatedness. In both bi-parental and cooperative groups, a female's engaging in extra-pair mating was independent of relatedness to her social mate; however, females preferred extra-pair sires to which they were more related than to their social mates. Moreover, females had higher relatedness with either their extra-group extra-pair sires in both bi-parental and cooperative groups, or within-group helper sires in cooperative groups, than expected by chance. When more than one potential extra-pair partner was available around a female's nest, she tended to select a relative. There was no indication of fitness reduction from extra-pair mating, which occurred at an intermediate level of inbreeding. These data support the kin-selection hypothesis, although there might be alternative nongenetic reasons associated with the extra-pair mating preference. Our finding offers a new explanation for why female birds pursue extra-pair mating. It also may broaden our understanding of the role of kin-selection in the evolution of cooperative society.     

Polymorphic signals of harassed female odonates and the males that learn them support a novel frequency-dependent model

For mate-searching species, the learned mate recognition (LMR) hypothesis assumes that sexual harassment favours signal variation among females, which exploits the receiver ability of males. The model predicts that coevolving males have responded to the female sexual foil by learning to recognize female variants as potential mates. I translate the LMR hypothesis into the language of signal detection theory to explain its novelty as a dynamic, coevolutionary, negative frequency-dependent selection model. Due to gene-environment interactions, males cueing to the morph detected most often should generate positive but often asymmetrical, detection-dependent harassment towards females. Females are expected to sort to an ideal free distribution where harassment costs are equal. At equilibrium, morph fitness, but not necessarily morph frequency, is predicted to be equal. The LMR hypothesis is consistent with recent experimental data and the distribution of colour polymorphisms in the Odonata, predicts general conditions favouring variation in sexual signals, and provides a novel mechanism for speciation via sexual signalling.     

Female reproductive strategies in orangutans,evidence for female choice and counterstrategies to infanticide in a species with frequent sexual coercion

Intersexual conflicts over mating can engender antagonistic coevolution of strategies, such as coercion by males and selective resistance by females. Orangutans are exceptional among mammals for their high levels of forced copulation. This has typically been viewed as an alternative mating tactic used by the competitively disadvantaged unflanged male morph, with little understanding of how female strategies may have shaped and responded to this behaviour. Here, we show that male morph is not by itself a good predictor of mating dynamics in wild Bornean orangutans but that female conception risk mediated the occurrence and quality of male–female interactions. Near ovulation, females mated cooperatively only with prime flanged males who they encountered at higher rates. When conception risk was low, willingness to associate and mate with non-prime males increased. Our results support the hypothesis that, together with concealed ovulation, facultative association is a mechanism of female choice in a species in which females can rarely avoid coercive mating attempts. Female resistance, which reduced copulation time, may provide an additional mechanism for mate selection. However, coercive factors were also important as prime males were frequently aggressive to females and females used mating strategies consistent with infanticide avoidance.     

Extreme polymorphism in a Y-linked sexually selected trait

Males of the livebearing fish, Poecilia parae, exhibit one of the most complex polymorphisms known to occur within populations, whereas females are monomorphic. We describe five distinct male colour morphs and an associated size dimorphism, and demonstrate through pedigree analysis that the locus or loci controlling the male colour polymorphism is linked to the Y-chromosome. Field surveys from 1999 to 2002 of nine populations in Guyana and Suriname, South America, indicate that some morphs are consistently abundant and others are rare, implying that the colour polymorphism has important fitness consequences. By rearing offspring of field-inseminated females, we showed that the common morph is also the most successful morph in terms of reproduction. However, dichotomous choice tests show that two rare morphs are preferred by females over the common morph. These results suggest that alternative male mating strategies, sperm competition, overt male-male competition, or other processes are overriding female preferences in these populations. Furthermore, Y-linkage of the colour polymorphism in P. parae supports the hypothesis that heterogametic sex chromosomes harbour sexually antagonistic traits beneficial to the heterogametic sex.     

The evolution of female‐limited polymorphisms in damselflies: a signal detection model

Female‐limited intraspecific colour variation is a widely distributed trait within damselflies. Typically, one morph resembles the male (the andromorph) whereas one, or sometimes more, do not [the heteromorph(s)]. While several selective explanations have been offered, such as decreased harassment by males balanced by predation or lack of mating success, field data indicate that andromorphs and heteromorphs mate at equal frequencies in the field, and survive equally well. In this paper, I use a signal detection model to characterize the properties of a new male‐mimicry hypothesis, in which andromorphs are not only more similar to males, but are also encountered more by males. I show that this combination of frequency‐dependent and frequency‐independent factors readily combine to generate a balanced polymorphism. The model explains why morphs have similar mean mating frequencies, why the experimentally observed mating preferences of males vary between ponds, and why the frequency of andromorphs tends to rise with sex ratio.     

No genetic correlation between the sexes in mating frequency in the bean beetle, Callosobruchus chinensis

Female multiple mating, which is common in animals, may have evolved not in response to fitness advantages to females but as a genetic corollary to selection on males to mate frequently. This nonadaptive hypothesis assumes a genetic correlation between females and males in mating frequency, which has received a few empirical investigations. We tested this hypothesis by observing the correlated response in male mating frequency in the adzuki bean beetle, Callosobruchus chinensis to artificial selection on female propensity to remate. Compared to control females, females from lines selected for increased or decreased female propensity to remate had, respectively, higher or lower mating frequency measured by the number of mating within a given period. This indicates that female receptivity to remating is genetically correlated with female mating frequency, and thus the artificial selection for female propensity to remate influenced female mating frequency. In contrast, males from the selected lines that diverged in female mating frequency did not vary significantly in their mating frequency. These results indicate that there is no genetic correlation between the sexes in mating frequency in C. chinensis. This study shows that the reason why females in C. chinensis remate despite suffering fitness costs cannot be explained by indirect selection resulting from selection on males to mate multiple times.     

Male mate choice based on ontogenetic colour changes of females in the damselfly <Emphasis Type="Italic">Ischnura senegalensis</Emphasis>

While male mate choice behaviour has been reported in many taxa, little is known about its plasticity and evolutionary consequences. In the damselfly Ischnura senegalensis, females exhibit colour dimorphism (gynomorph and andromorph). The body colour of gynomorphs changed ontogenetically in accordance with sexual maturation, while little change occurred in andromorphs. To test the male mate choice between sexually immature and mature females of both morphs, binary choice experiments were conducted. Virgin males that were reared separately from females after emergence did not show significant preference between sexually immature and mature females for both morphs, indicating that virgin males were unable to discriminate female reproductive status. On the other hand, males that had experienced copulation with gynomorphs preferred sexually mature gynomorphs to sexually immature ones. However, males that had experienced copulation with andromorphs could not discriminate between sexually immature and mature andromorphs, probably due to the absence of significant ontogenetic change in their thoracic colour. Therefore, female body colour is an important cue for males in discriminating between sexual maturation stages. Learned mate discrimination depending on copulation experience might help males to detect potential mates effectively and avoid sexually unreceptive immature female. We finally discuss the adaptive significance of the ontogenetic colour change in females.