Male-like Females Research Articles

Evolving social dynamics prime thermal tolerance during a poleward range shift

Cold tolerance plays a critical role in determining species geographical range limits. Previous studies have found that range shifts in response to climate warming are facilitated by cold acclimation capacities, due to increasingly colder and variable weather at high latitudes, and that cold tolerance can also be influenced by social factors. In this study we combined experiments and field studies to investigate the climatic and social factors affecting cold tolerances in range- shifting populations of the female-polymorphic damselfly Ischnura elegans in northeast Scotland. In the field, we observed both environmental (measured via habitat suitability) and social (sex ratio and density) effects on cold tolerance (CTmin). Androchrome females (male-like females) were less susceptible to beneficial social effects on cold tolerance than gynochromes (female- like females), and correspondingly, gynochrome frequency increased at colder, environmentally- limiting sites towards the range margin. Our manipulations of density in the laboratory further provide novel, experimental evidence that social interactions directly impact cold tolerance n this species. These results suggest that reciprocal effects of social environments on thermal acclimation may be an important but commonly overlooked aspect of allee effects which contribute to the formation of range margins. Moreover, our results point to a wider need to consider the role of population and social dynamics to shape both the thermal physiology of individuals and the thermal niches of species.

Adaptive significance of permanent female mimicry in a bird of prey

Permanent female mimicry, in which adult males express a female phenotype, is known only from two bird species. A likely benefit of female mimicry is reduced intrasexual competition, allowing female-like males to access breeding resources while avoiding costly fights with typical territorial males. We tested this hypothesis in a population of marsh harriers Circus aeruginosus in which approximately 40 per cent of sexually mature males exhibit a permanent, i.e. lifelong, female plumage phenotype. Using simulated territorial intrusions, we measured aggressive responses of breeding males towards conspecific decoys of females, female-like males and typical males. We show that aggressive responses varied with both the type of decoys and the type of defending male. Typical males were aggressive towards typical male decoys more than they were towards female-like male decoys; female-like male decoys were attacked at a rate similar to that of female decoys. By contrast, female-like males tolerated male decoys (both typical and female-like) and directed their aggression towards female decoys. Thus, agonistic responses were intrasexual in typical males but intersexual in female-like males, indicating that the latter not only look like females but also behave like them when defending breeding resources. When intrasexual aggression is high, permanent female mimicry is arguably adaptive and could be seen as a permanent 'non-aggression pact' with other males.

Interpopulational variation of the mating system in the peacock blenny Salaria pavo

The ecology and mating system of two populations of the peacock blenny Salaria pavo that have been reported to differ in sexual behaviour were studied. In the Gulf of Trieste, a northern Adriatic Sea population lives in rocky shores, whilst in the Ria Formosa, an Atlantic population inhabits a coastal lagoon with sandy barrier islands. In the Gulf of Trieste, nest availability was found to be higher and nest aggregation lower than in Ria Formosa. Nesting males courted females more and in higher proportion, and inversely, females directed less courtship displays towards nest holders in the Gulf of Trieste than in Ria Formosa. The relative frequency of small female-like males that reproduce by parasitically fertilizing eggs in the larger males’ nests was lower in the Gulf of Trieste population. This variation in the sexual behaviour of nesting males and females is likely to reflect a plastic behavioural response to the varying ecological conditions. The difference between populations in the relative frequency of parasitic males suggests that the male alternative reproductive tactics are condition-dependent.

Frequency-dependent variation in mimetic fidelity in an intraspecific mimicry system.

Contemporary theory predicts that the degree of mimetic similarity of mimics towards their model should increase as the mimic/model ratio increases. Thus, when the mimic/model ratio is high, then the mimic has to resemble the model very closely to still gain protection from the signal receiver. To date, empirical evidence of this effect is limited to a single example where mimicry occurs between species. Here, for the first time, we test whether mimetic fidelity varies with mimic/model ratios in an intraspecific mimicry system, in which signal receivers are the same species as the mimics and models. To this end, we studied a polymorphic damselfly with a single male phenotype and two female morphs, in which one morph resembles the male phenotype while the other does not. Phenotypic similarity of males to both female morphs was quantified using morphometric data for multiple populations with varying mimic/model ratios repeated over a 3 year period. Our results demonstrate that male-like females were overall closer in size to males than the other female morph. Furthermore, the extent of morphological similarity between male-like females and males, measured as Mahalanobis distances, was frequency-dependent in the direction predicted. Hence, this study provides direct quantitative support for the prediction that the mimetic similarity of mimics to their models increases as the mimic/model ratio increases. We suggest that the phenomenon may be widespread in a range of mimicry systems.

Reflectance spectra and mating patterns support intraspecific mimicry in the colour polymorphic damselfly Ischnura elegans

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.

Sex‐dependent selection on an autosomal melanic female ornament promotes the evolution of sex ratio bias

Sex-dependent selection often leads to spectacularly different phenotypes in males and females. In species in which sexual dimorphism is not complete, it is unclear which benefits females and males derive from displaying a trait that is typical of the other sex. In barn owls (Tyto alba), females exhibit on average larger black eumelanic spots than males but members of the two sexes display this trait in the same range of possible values. In a 12-year study, we show that selection exerted on spot size directly or on genetically correlated traits strongly favoured females with large spots and weakly favoured males with small spots. Intense directional selection on females caused an increase in spot diameter in the population over the study period. This increase is due to a change in the autosomal genes underlying the expression of eumelanic spots but not of sex-linked genes. Female-like males produced more daughters than sons, while male-like females produced more sons than daughters when mated to a small-spotted male. These sex ratio biases appear adaptive because sons of male-like females and daughters of female-like males had above-average survival. This demonstrates that selection exerted against individuals displaying a trait that is typical of the other sex promoted the evolution of specific life history strategies that enhance their fitness. This may explain why in many organisms sexual dimorphism is often not complete.

Brain aromatase mRNA expression in two populations of the peacock blenny Salaria pavo with divergent mating systems

Aromatase, the key enzyme in the conversion of androgens to estrogens, regulates the availability of these hormones in tissues and controls many physiological and behavioral processes. In fish and other vertebrates, the regulation of aromatase expression in the brain has been implicated in the modulation of male sexual and aggressive behaviors. Here, the pattern of mRNA expression of the brain aromatase isoform (encoded by the CYP19A2 gene also referred as CYP19b) was quantified at the peak of spawning season in brain macroareas from males and females of the blenny Salaria pavo originated from two populations displaying male alternative reproductive tactics but differing in their mating systems. In Trieste (Adriatic) nesting males aggressively defend nests and take the initiative in courtship and perform sexual displays more often than females while in Ria Formosa (Southern Portugal) the pattern is reversed as a result of shortage of appropriate nesting sites. Nesting males from Ria Formosa had overall higher levels of brain aromatase mRNA expression than nesting males from Trieste, suggesting a higher brain estrogen synthesis in these males. Since in some fish species exogenous estradiol administration has been shown to decrease sexual and agonistic behaviors, the higher levels of brain aromatase in Ria Formosa nesting males may explain their reduced expression of sexual and aggressive displays when compared with nesting males from Trieste. Alternatively, the higher brain aromatase levels in nesting males from Ria Formosa could be a mechanism to decrease the putative androgen-induced activation of aggressive and sexual displays by reducing the local availability of androgens through their metabolization into estrogens. Although females and parasitic female-like males also differ in their displays between populations, the interpopulational pattern of brain aromatase mRNA expression was similar, suggesting that other neuroendocrine agents mediate the expression of female and female-like behaviors. In conclusion, brain aromatase availability seems like a probable mechanism to regulate the effects of steroids on the brain circuits underlying the expression of sexual and agonistic displays in S. pavo.

Female-limited polymorphism in a widespread damselfly: morph frequencies, male density, and phenotypic similarity of andromorphs to males

In several animal species, one male type coexists with two to several female types, a polymorphism often explained in the context of sexual selection. Where it occurs, one female morph typically resembles the conspecific male phenotype, but the degree of resemblance varies across species. Here, we question whether the degree of phenotypic similarity between male-like females and males varies within species. Phenotypic resemblance is hypothesized to depend on the potential for frequency- and density-dependent selection on male and (or) female phenotypes. We studied six populations of the damselfly Nehalennia irene (Hagen, 1861) that differed widely in estimates of morph frequency and male density. Male-like females resemble males more than another female type resembles males, across populations, when comparisons are based on abdominal patterns. Abdomen phenotype does matter in male–female interactions of damselflies. Furthermore, male-like females were more similar to males at low and high density sites compared with sites with intermediate densities, contrary to the hypothesis that the potential for male harassment influences the degree of phenotypic similarity. Additionally, male-like females of most populations converged on the abdominal phenotype of males of one population rather than on that of syntopic males; a problem that has not received any attention.

Male-like females of a damselfly are not preferred by males even if they are the majority morph

Animals searching for prey and males searching for mates share similar problems of detection if their targets are diverse in colour or physical appearance. There is good evidence for predators switching their preferences for prey in a frequency-dependent way; predators focus on the most common form, and the decreased predation on rarer forms allows multiple forms to survive. Frequency-dependent mate selection has also been proposed to explain the maintenance of several female colour morphs in damselflies. However, the fact that one of the female morphs is coloured like a male (androchrome) and behaves similarly to males suggests the phenomenon of male mimicry in this system as an alternative explanation for the polymorphism. We compared androchrome frequencies in populations and mating pairs in Ischnura elegans, over a range of androchrome frequencies (8–90%). In 22 of 23 samples androchromes mated less often than expected (significantly in 13 samples). We found no evidence for males switching their preferences in a frequency-dependent way. A test of male preference for female morphs in a population with 85% androchromes indicated that males behaved indiscriminately and did not prefer the commonest (male-like) morph. Our results support androchrome male mimicry rather than learned mate recognition by males (a purely frequency-dependent model) as the main mechanism behind the maintenance of this sex-limited colour polymorphism.

The evolution and frequency of female color morphs in Holarctic Odonata: why are male-like females typically the minority?

Abstract We compiled data on the occurrence and frequency of distinct female variants among Holarctic Odonata and interpreted the data in light of harassment-based hypotheses. The major source of male confusion for male mimicry hypotheses is predicted to be signal similarity between andromorphs and male distractors; for the learned mate recognition hypothesis (LMR), it is predicted to be variation in female signals. Mapping morphism state onto molecular phylogenies of Ischnura and Enallagma failed to resolve the general ancestral female condition. However, it appeared that the andromorphic state may be ancestral in one case, and that blue structural colors were ancestral to orange and green pigmentations. Of the polymorphic species surveyed, 13% had more than two morphs, 4% had multiple heteromorphs but no andromorph, and 7% of ‘monomorphic’ congeners were functionally polymorphic because developmental variants mate. Such female signal variation lies beyond the scope of simple male mimicry, but neverthele...

The adrenocortical responses to stress in breeding male Chaffinches Fringilla coelebs and Bramblings F. montifringilia in Sweden

There is growing evidence that birds, and possibly other vertebrates, modulate the adrenocortical response to acute stress as measured by increases in plasma levels of corticosterone following capture and handling. Field-endocrine investigations of these adrenocortical responses to capture stress have begun to indicate ecological bases for such endocrine phenomena. One hypothesis states that populations of birds breeding under extreme conditions such as in Arctic and subarctic habitats, where the breeding season also is short, should suppress the adrenocortical response to acute stress so as to allow onset of breeding under potentially severe conditions. To test this we measured increases in circulating levels of corticosterone following capture and handling in a population of male Chaffinches Fringilla coelebs breeding in southern Sweden. The dynamics of changes in corticosterone levels during this capture stress protocol were compared with those collected from male Brambling F. montifrigilla breeding in a subalpine habitat in northern Sweden where conditions are more severe and the breeding season short. Contrary to the predictions, male Bramblings showed a greater adrenocortical response to stress as indicated by the pattern of corticosterone levels in blood. Both male Bramblings and Chaffinches show marked individual variations in the pattern of corticosterone changes following capture. In Chaffinches the initial corticosterone were negatively correlated with body mass and body size expressed as ratio of body mass to wing length cubed. The percent increase in corticosterone and maximum levels were also correlated with fat score. Male Bramblings showed no relationship of corticosterone dynamics with body condition. Furthermore, there was no relationship to plumage variability (i.e. from black plumage on the head and upper thorax to grey, streaked, female-like males). Although several avian species have been shown to reduce their adrenocortical responsiveness to acute stress in severe environments, these data suggest that other factors may regulate the hypothalamo-pituitary-adrenal cortex axis as well.

Reversible frequency-dependent switches in male mate choice.

Current sexual-selection theories predict that mating should occur preferentially with the highest-quality partner, and assume that for distinguishing among potential mates the choosy sex applies an internal representation of the characteristics of the desired mate, i.e. a template. Binary choice experiments were performed to test male mate choice between two different female colour morphs in the damselfly Ischnura elegans. Choice experiments were conducted before and after an habituation period, during which males were exposed to only one female colour morph. Given the choice between the two female morphs, males did exhibit a choice for the most recently experienced female morph. This is the first evidence for a reversible switch in mate choice in a frequency-dependent way. In contrast with previous studies on mate choice, template formation in male I. elegans seems not to be based on quality. Switching mate choice in a frequency-dependent manner, choosing the most common morph, probably allows males to minimize their search efforts and to maximize fitness.

Male aggressiveness and the possible occurrence of group territoriality in the Brambling Fringilla montifringilla

Bramblings are nomadic birds with an interesting breeding ecology. Their nests are often aggregated in groups of two to eight nests. Such aggregated nesting may indicate the existence of group territories, probably formed for anti-predatory purposes. The male Bramblings show much variation in colour pattern during the breeding season, with individuals ranging from completely black-hooded to virtually female-like grey-hooded. The colour pattern is probably age dependent, but may also be correlated with social status. The present study of breeding Bramblings was performed during the summer 1998 at Ammarnäs, County of Västerbotten, Sweden. We simulated an intrusion in the breeding territory, using an artificial intruder (a decoy) and a tape recorder with Brambling song, to find evidence for the group territory hypothesis and to investigate the possible correlation between male plumage pattern and aggressiveness. Only intermediate males (type 2) and black-hooded males (type 1) (i.e. no female-like males), were observed during experiments at 13 nests. The type 2 males were slightly more active and aggressive towards the intruder-decoy (an intermediate male), when tested close to the nest, than were the type 1 males. The decoy was never attacked by more than one male at a time, but there were more than one male present in 77% of the experiments, which does not exclude the possibility for the existence of a group territory.

The Significance of Female Mimicry in Male Contests

In many animal species, the two sexes are very similar in appearance. One hypothesis for such sexual indistinguishability is that the members of one sex benefit from resembling those of the other sex. Here we focus on the adaptive significance for males of resembling females. We suggest that female mimicry may directly enhance the competitive ability of a male. This is because males that conceal their sexual status may hide important information to their opponent (i.e., that they are males and represent a threat). We use game theory to present this hypothesis. The hypothesis is supported in an experiment with pied flycatchers (Ficedula hypoleuca), a species that previously has been shown to have difficulties in discriminating between female-like males and females. In aviary trials involving contests between black males and female-like males over a nest site, we show that female-like males were the first of the competitors to initiate attacks and were also the winner of the contest in nearly all cases. The same result was found when we used two female-like males of which one was painted black. Apparently, female-like males gain an advantage because they are in control of when to initiate a fight because of the opponent's poor sex recognition ability. We discuss our hypothesis in relation to delayed plumage maturation theory and the evolution of sexual indistinguishability. We suggest that concealment of sex in competitive interactions may be especially relevant to animals in which males provide resources that are attractive to females, such as a territory or a nuptial gift. In such cases, resource-holding males may benefit from signaling their true sex in order to attract females, whereas male intruders may benefit from concealing their sex. Concealment of sex would be easy to achieve in species in which sexual signaling is canalized through nonpermanent signals. However, female mimicry may also be evolutionarily stable in animals in which a high proportion of resource-holding males possess permanent sexual signals but intruders mimic the sexual signals of females-that is, if social status is relatively highly predictable. Examples of the latter situation may be exemplified by some bird species that possess delayed plumage maturation.

Male coloration and species recognition in sympatric flycatchers

Currently favoured views for explaining ornaments in males emphasize female preference such that females benefit from increased offspring production, good genes of the offspring, or the attractiveness of sons. Results from long-term studies in the pied flycatcher Ficedula hypoleuca suggest that factors associated with species recognition may also be important for male coloration. In sympatry the collared flycatcher F. albicollis is dominant in competition for nesting sites over the pied flycatcher. Bright pied flycatcher males resemble collared flycatcher males and suffer from interspecific interference, whereas dull and female-like males can acquire nesting sites close to those of the collared flycatcher. (A similar aggression release mechanism had previously been suggested to influence the evolution of colour differences in coral reef fishes.) Additionally, the risk of hybridization was low for the dullest pied flycatcher males, resurrecting the idea that avoiding mating with wrong species might currently be under selection. Thus interspecific effects related to species recognition can probably explain the dull plumage colour of pied flycatcher males in sympatry. In allopatry, intraspecific sexual selection for bright coloration in males seems to be weak, and even a low level of gene flow between sympatric and allopatric populations may maintain the high variation in this highly heritable trait.

Mate choice in the polymorphic African swallowtail butterfly, Papilio dardanus: male-like females may avoid sexual harassment

Abstract. Papilio dardanus, the African swallowtail butterfly, is a species with a female-limited polymorphism for wing colour pattern. Females of the subspecies P. dardanus tibullus on Pemba Island, Tanzania, occur as three genetically distinct morphs; a black and white Batesian mimic ( hippocoonides), a black and yellow male-like morph ( trimeni) and a morph that is similar to trimeni but with orange wing-patches ( lamborni). Male mate choice was studied by recording the responses of wild males first to simultaneously presented pairs of pinned dead females, second, in sequential choice tests where only a single female was presented at a time, and third, during focal follows of wild females. From a distance males consistently preferred the Batesian mimic, hippocoonides, above the andromorph, trimeni, and trimeni above the third morph lamborni . Preference correlated both with the frequencies of the morphs and their colour, the more common brighter morphs being preferred. It is proposed that the hippocoonides, trimeni and possibly also lamborni morphs are maintained in a stable polymorphism by different frequency-dependent selective advantages. The morph hippocoonides supposedly have low predation because of Batesian mimicry (frequency-dependent) but suffer costly harassment by males, whereas trimeni avoid this harassment through male mimicry (possibly also a frequency-dependent advantage) but are not protected from predators. The third morph, lamborni, which suffers the lowest levels of harassment, may gain this advantage by mimicking the orange coloration of ageing males.

Evidence for sex recognition from plumage colour by the pied flycatcher, Ficedula hypoleuca

In sexually dichromatic birds, plumage colour is assumed to be an important cue for sex recognition, yet little critical evidence so far exists to support this assumption. Using live, caged birds the sex recognition ability of pied flycatchers was tested. A female, painted black to resemble a male, was treated by territorial, unmated males as if she were a male; this also occurred when the painted female was presented to mated males and females. A male with a natural plumage colour resembling that of a female was treated by unmated males as if he were a female. The latter response did not change even when male song was played from a loudspeaker placed beneath the caged bird. However, when the female-like male was again presented, after being painted black, the resident males treated him as a male. Hence, in sexual recognition by this species, plumage colour provides an important cue. This makes it possible for female-like males to deceive conspecifics about their true sexual status.

Widespread polychromatism in female sunangel hummingbirds (Heliangelus: Trochilidae)

In hummingbirds, a showy gorget of iridescent throat feathers is a characteristic male ornament in many sexually dichromatic species. Given that polygynous breeding systems are the only ones observed in hummingbirds, and that polygyny is often associated with dramatic male ornamentation and sexual dimorphism, it is not surprising that gorgets are usually interpreted as sexual display characters. This proposition is challenged by exceptional ‘polychromatic’ species in which adult females diner in their development of a male-like gorget. This analysis focuses on determining the prevalence of polychromatic variation in the Andean genus Heliangelus. In eight of nine species, females' gorgets range from a dull plumage characteristic of most female hummingbirds (female-like), to a bright iridescent plumage that matches that of the males (male-like). Analysis of museum study-skins reveals that individual variation in gorget colour is limited to females, and that it is independent of month and year of collection. Only H. exortis and H. amethysticollis exhibit significant geographic variation in the frequencies of different colour forms, though most male-like female H. amethysticollis occur in southern Ecuador-northern Peru. Some species-specific features of the male-like females' gorget appear to be linked to qualities of the male gorget (presence/absence, colour and maximum size). However, non-adaptive hypotheses, including genetic correlation between the sexes, hybridization and neutral variation, cannot account for the plumage variation among females. The absence of any association between female gorget colour and breeding condition suggests that gorget colour has a non-sexual function. I propose that gorgets can evolve solely as a non-sexual signal associated with different foraging behaviours.

EVOLUTION OF PLUMAGE COLOR IN MALE PIED FLYCATCHERS (FICEDULA HYPOLEUCA): EVIDENCE FOR FEMALE MIMICRY.

We present the first evidence for sexual deception by female mimicry in birds. Using live, caged birds we show that territorial male pied flycatchers behave aggressively toward bright-colored males but display sexually toward female-like male intruders. We also show that the males that are fooled are those that lack recent sexual experience. All male pied flycatchers are dull-colored in winter. It is possible that young males are more constrained during the spring molt than older males since the former are more dull-colored in spring. According to the molt-constraints hypothesis a subadult plumage would be maladaptive in the breeding season. Analysis of male settling pattern at breeding sites in spring suggests that brownish males are allowed to settle closer to already-established males than dark-colored males. This result suggests an adaptive value of having a subadult plumage color, in particular for young males arriving late from spring migration. However, we also show that mimicry incurs a cost, that of increased aggression from females, which may explain why female-like males have reduced mating success.

Intrapopulation Variation in the Breeding of Male Pink Salmon (Oncorhynchus gorbuscha) from a Lake Superior Tributary

Studies of breeding pink salmon (Oncorhynchus gorbuscha) from the Carp River, eastern Lake Superior, indicate that males seek fertilizations using two behavioural tactics. In 1985, a large run resulted in high breeding ground densities. During this run, males that resembled females were seen seeking fertilizations by sneaking rather than by competing for proximity to females. Morphological studies in 1985 confirmed the presence of males resembling females, their secondary sexual characters (hump height) being relatively less developed than in typical males. Although in poorer condition, such female-like males were reproductively mature, had returned to spawn at ages typical for this population, and had committed biomass to gonad no differently than had typical males. Furthermore, their spawning performance did not differ from typical males, as assessed both by the amount of gonad they retained unspawned at death and by their spawning ground life expectancies. In contrast, males attempting to sneak fertilizations were not observed during the small 1984 run when densities were low and males were generally in better condition than in 1985. Together, these results indicate that male pink salmon exhibit alternative breeding tactics. However, the demonstration of these tactics appears linked more to proximate factors (density and condition) than to divergent life history strategies as in other salmonid species.