Male mate choice favors more colorful females in the gift-giving cabbage butterfly

While the phenomenon of male mate choice has attracted considerable attention in the last two decades, whether this sexual selection mechanism could drive the evolution of female ornaments remains poorly understood. Here, we used experimental manipulation of female wing coloration to investigate male mate choice in Pieris rapae, a gift-giving butterfly. Further, we tested whether males’ nutritional status influenced their mating preferences by subjecting larvae to short periods of starvation. We found that males showed significantly more mating approaches toward control females with more colorful wings (higher pteridine content), and that this preference was strongest in low-nutrition males. Additionally, a study of field-collected females revealed that pteridine-based wing coloration was positively correlated with female egg load, which suggests such ornaments may signal female quality. Pteridine-based ornaments are widespread in nature, however their potential as honest signals in male mate choice remains largely unexplored. This work furthers our understanding of how male mate choice and female ornamentation may evolve in species whose mating systems include nutritional nuptial gifts.     

Context-dependent genetic benefits of extra-pair mate choice in a socially monogamous passerine

Extra-pair paternity is common in socially monogamous passerines; however, despite considerable research attention, consistent differences in fitness between within-pair offspring (WPO) and extra-pair offspring (EPO) have not been demonstrated. Recent evidence indicates that differences between maternal half-siblings may depend on environmental conditions, but it is unclear whether the influence of paternal genetic contribution should be most apparent under comparatively poor or favourable conditions. We compared phenotypic characteristics of WPO and EPO in 30 mixed-paternity broods of the tree swallow (Tachycineta bicolor) in relation to experimentally increased nest temperature (n = 13 heated nests; 17 control nests) and natural abundance of haematophagous parasites (Protocalliphora spp.). This allowed us to test the hypothesis that genetic benefits of extra-pair mating are environment dependent. EPO grew their ninth primary feathers faster than WPO regardless of nest temperature or parasite load and had significantly longer ninth primary feathers at fledging when parasite abundance was low, and when they were positioned early in the hatching sequence relative to WPO. In contrast, WPO under similar conditions did not differ from EPO in any phenotypic trait measured. These results indicate that the fitness benefits of extra-pair mating are likely to be context dependent, and that genetic effects on some phenotypic traits may be more apparent when conditions are relatively favourable.     

Potential direct fitness consequences of ornament-based mate choice in a butterfly

Female mate choice has been shown to provide direct mating benefits in several animal groups. In butterflies, for which there are increasing reports of fine-scale color-based mate choice, the evolutionary benefits that accrue from such mating biases, if any, are largely unknown. We addressed this issue in the butterfly Colias eurytheme, a species in which females choose mates on the basis of iridescent ultraviolet (UV) wing ornamentation and in which males donate reproductively beneficial nuptial gifts. In the first experiment, we assessed the mass of gifts donated to 77 virgin females by males sampled directly from a field encounter site. Despite large variance in the male adult phenotype and ejaculate, no single aspect of dorsal wing coloration, including UV brightness, chroma, or hue, was related to ejaculate mass. There was, however, an interesting interaction between the effects of male body size and copula duration upon ejaculate mass, with size scaling positively with ejaculate mass among males involved in shorter copulations (those lasting <70 min) but negatively among males in longer copulations. In the second experiment, we assessed the lifetime fecundity, fertility, and longevity of 85 females mated under similar circumstances to free-flying wild males. Although several wing color parameters proved subtly informative in more sophisticated multivariable models, no model predicted more than about 20% of the variation in any single female fitness parameter. The duration of copulation, which ranged from 35 min to over 16 h and which carries putative costs for females, was, again, only very weakly predicted by male wing color parameters (i.e., R ² = 0.089). Given the overall minor predictive power of male wing coloration in general and of UV brightness in particular, our results do not strongly support the hypothesis that female C. eurytheme prefer bright UV males to obtain direct benefits or to minimize the costs associated with lengthy copulations.     

No male agonistic experience effect on pre-copulatory mate choice in female earwigs

Mating with dominant males may confer considerable benefits, but also incur significant costs, hence intrasexual competitiveness is a likely target of mate choice. In addition to established modes of mate assessment, females may use cues or signals associated with agonistic experience effects to assess the relative competiveness of males. Experience effects, where the outcome of a fight increases the likelihood of a similar outcome in subsequent fights, may result from an animal’s altered state after conflict, but can also arise from strategic rival use of information perceived about this altered state. While females may similarly use this information in mate choice decisions, this potential consequence of male–male conflict has largely been neglected. Here, we investigate the effects of experience on subsequent agonistic performance in the earwig Euborellia brunneri by imposing winning or losing experiences on males and rematching them with naïve, size-matched rivals. We reveal a strong loser effect in subsequent fights, with nearly all previous “losers” losing against new rivals. In contrast, we found no equivalent winner effect, with previous “winners” exhibiting no increased likelihood of winning. We subsequently test whether the effects of male agonistic experience extend to pre-copulatory female mate choice. We show that females, when allowed to choose between naïve males and “winners” or “losers”, do not discriminate between males based on their recent agonistic experience. Therefore, while fighting history can play an important role in male–male interactions, females may not attend to this information.     

Behaviour and choice of refuge by voles under predation risk

Animals often show a strong antipredatory response when they are exposed to their most deadly predator. In northern vole populations, the least weasel, Mustela nivalis nivalis, is probably the most important predator of voles. Because of its small size and slender body shape, the least weasel is capable of hunting voles in their burrows. However, small voles can potentially escape weasel predation by selecting holes smaller than those weasels can enter. We studied the choice of nest holes and refuges by two species of voles under simulated predation risk. In a laboratory experiment, voles were provided with four nest boxes as refuges, with individually adjusted entrance sizes. When exposed to the odour of a weasel, voles did not choose the smallest opening; they rather seemed to trade full protection for easy and immediate access by choosing the nest box with an intermediate entrance size. When outside the nest at the time when a weasel entered the arena, voles avoided the refuges with the smallest holes. In addition to using refuges on ground level, voles climbed on top of the boxes as an escape reaction, as well as exhibiting a variety of behavioural responses, such as fast running, freezing and sneaking.Communicated by P.A. Bednekoff     

Perceived predation risk and mate defense jointly alter the outcome of territorial fights

Virtually all animal conflicts occur over access to mates or resources that affect survival, the two key components of fitness. In this paper, we report that predation risk and mate defense jointly affect the outcomes of contests between male sand crabs (Scopimera globosa) for burrows in which crabs mate and take shelter from predators. We observed the contests under three different conditions: (1) the natural condition of low predation risk and without the presence of a female; (2) the first experiment in which we imposed upon only intruding males the perception of predation risk—by digging them from their burrows, capturing and handling them, and placing them into other males’ burrows—to increase the value of the burrows for the intruders as shelter, and (3) the second experiment in which we repeated this treatment but increased the resource value of the burrow to the resident by placing a female in his burrow. The difference in body size between contestants was the main determinant of victory in all analyses. However, perceived predation risk also partly affected the outcomes of the fights: The motivated intruders were likely to win even when they were a little smaller than the residents. In addition, defense of a female had a significant effect on the outcomes of fights: The motivated residents won more fights than the motivated intruders, indicating that these two treatments caused asymmetric increases of the resource value. This is the first report of two external factors simultaneously raising resource value, affecting motivation of contestants, and altering the outcome of fights.     

Fitness benefits of multiple mating versus female mate choice in the cellar spider (Pholcus phalangioides)

Recent studies have demonstrated that mating with multiple males can be beneficial for females and her offspring even if males contribute nothing but sperm. This was mainly established for species in which sperm from several males mix in the reproductive tract of the female, thus allowing sperm competition and/or female sperm choice. However, in species with last male sperm precedence, female re-mating decides against the previous male by strongly limiting his reproductive success. We tested the effect of female re-mating behaviour using the cellar spider Pholcus phalangioides, which shows strong last males sperm precedence and moderate levels of polyandry under natural situations. We predicted that females prevented from remating even though they are receptive would show reduced reproductive success compared to females that accept two copulations and females that reject a second male, since the latter two treatments were allowed to behave according to their decisions. However, if the number of matings per se had an effect on oviposition or on offspring performance, double-mated females should perform better compared to both treatments of once-mated females. We measured female fecundity and fertility over a period of 140 days, comparable to the species' natural reproductive peak season. Two thousand one hundred and fifty-two offspring from 67 first egg sacs were reared under two feeding levels. We registered development time and survival, and measured offspring adult size and mass. We found a positive effect of double mating, as in this treatment, oviposition probability was higher compared to the other treatments. Interestingly, adult female offspring of the DM treatment that were raised under low food level had a higher condition index compared to those from FS and RM, but development time, size and mass at adulthood were not affected by mating treatment. Female choice only seemed to affect hatching latency of the offspring. Overall, the main predictor of female reproductive output and success was female body size.     

Strategies of female mate choice: A theoretical analysis

Summary Females of many species face a difficult sampling problem while searching for a mate. How do they find the best male possible when the constraints of time, memory, and mobility prevent them from visiting all the males in the population?Five possible solutions are examined: random mating a fixed-threshold criterion, a fixed-threshold with last-chance option, an optimal one-step decision strategy, and the best-of-n-males strategy. Random mating is the worst strategy whenever the female gets more than one chance to mate. The two fixed-threshold strategies approach equal effectiveness as n increases but are always below the optimal one-step decision strategy. However, the best-of-n-males strategy always yields the highest expectation of fitness in a mate. The difference is especially great when n5.Plotting the average fitness of males chosen vs n, the number of males examined, yields a negatively accelerating curve. Since the cost of searching will be an increasing function of n, the two curves can be combined to yield an optimum n: the point where the difference between the curves is greatest.The one field study (Brown 1978) that addresses these problems in detail reveals that female mottled sculpins choose males on a relative, rather than absolute, basis, as theory suggests they should.     

Non-independent mate choice in a fiddler crab: a case of stimulus enhancement

Non-independent mate selection occurs when the choice behavior of a female is altered by the interactions between other females and males. In the fiddler crab Uca mjoebergi, males court mate-searching females by waving their one greatly enlarged claw. When a female approaches a male, he initiates high-intensity waving. We conducted one natural mate choice experiment and two mate choice experiments using custom-built robotic crabs. We show that the decision of one female to approach a group of males increases the probability that another female will approach and visit a male from the same group. We suggest that this behavior is best explained by the ‘stimulus enhancement’ hypothesis, where the presence of a female near a group of males makes them more likely to be detected by other females due to an increase in male display rate.     

Measuring mate choice using correlation: the effect of female sampling behaviour

For intersexual selection to occur, it is necessary that females choose between males. It is now well appreciated that constraints exist, which preclude females sampling all the available males in a population. These constraints are likely to have caused the evolution of sampling rules (such as the “best-of-n” rule) by which females sample males. Here we investigate the impact of female subsampling of the male population, not on the evolution of sampling behaviour, but on the population-level correlation between a male trait and currencies such as reproductive success. This study is important as it illustrates when population-level correlations can be safely used to infer the presence and strength of sexual selection in the field. We find that the correlation between a male trait and a mate choice variable rises steeply as the number of males sampled by each female increases, flattening above seven to ten males sampled. This shape is found to be remarkably robust, and little affected by, for example, the mate choice variable used, by noise in assessment, by sampling behaviour depending on female quality, or by population size. The only variable found to have a large impact is male clumping according to their “quality”. If females are sampling about four males, the maximum correlation that can be found at the population level is in the range 0.4–0.6, perhaps as little as 0.1 if males are strongly clumped. A recent review of the literature suggests that four is the average number of males that females sample. Thus, the absence of a strong correlation cannot by itself be used to infer that sexual selection is weak, as it may be due to females sampling few males. Received: 18 May 1998 / Accepted after revision: 18 July 1998     

Uniform predation risk in nature: common,inconspicuous, and a source of error to predation risk experiments

Previous studies indicate that when predation risk is uniform across habitats, foragers concentrate their exploitation in fewer patches. Although uniform predation risk may seem rare in nature, some scenarios might cause it. Testing all scenarios in a single experiment is unfeasible; therefore, we developed a model that points whether concentration of exploitation in specific habitats due to uniform risk requires parameter values similar to what is found in literature. This model was based on Brown’s (Behav Ecol Sociobiol 22:37–47, 1988) fitness function but rescaled to multiple habitats and predators, including uniform risk predators. Deriving function’s maximum allowed comparisons with giving-up density studies. Results showed that uniform predation risk had a u-shaped effect in habitat exploitation, causing a concentration of habitat exploitation at probabilities of survival from 0.2 to 0.8. However, the length of this interval and degree of concentration depended on the value of safety to forager fitness. Heterogeneous, nonuniform, predation risk decreases habitat exploitation where it was higher, therefore suppressing the effect of uniform risk on prey behavior. Time spent in the focal habitat and metabolic costs reduced the detectability of habitat concentration, while total time did not. We also found that uniform risk reduced accuracy of heterogeneous risk measurements. Future studies should aim to control all possible predators, as even the mild ones can induce complex behavior.     

Active mate choice at cock-of-the-rock leks: tactics of sampling and comparison

Summary The importance of active mate choice as a component of sexual selection remains controversial, despite recent studies identifying traits that correlate with male mating success. We analyzed the sampling sequences of individual female Guianan cock-of-the-rock, providing quantitative documentation of active female choice in this lekbreeding species. We compared observed sampling patterns with null models of random female movement and of movement weighted by the observed distribution of male success. The courts actually visited by individual females were significantly more clumped and centrally located than predicted by computer simulations of either random or weighted movement. Contrary to simplified hypotheses of female choice, hen cock-of-the-rock were not limited either to sequential comparisons or to threshold decision rules when selecting mates. Instead, they repeatedly sampled a subset of potential mates, using the pool-comparison tactic. Within this pool, females preferentially mated with the males ranked highest in terms of total courtship visits received, and rejected low-ranking males. Our results suggest complex interactions between patterns of female sampling and male dispersion in lek mating systems, and also provide insights into the constraints on female sampling in lek species.     

Display rate by male fairy-wrens (Malurus cyaneus) during the fertile period of females has little influence on extra-pair mate choice

Empirical and theoretical studies have only recently begun to examine how females use complex multi-component displays when selecting mates. Superb fairy-wrens are well suited to the study of female choice because females have control over extra-group paternity and cuckold their mates at high rates, while males possess a variety of sexually selected traits. Available evidence suggests that females base their extra-group mate choice on the timing of male moult into breeding plumage or the onset of display. However, males continue to perform elaborate displays throughout the season, and direct most displays to females during their fertile period. We therefore conducted focal observations on fertile females to quantify the frequency of male display and used microsatellite genotyping to compare the role of display rate during the breeding season and the timing of male moult on female mate choice. We show that the addition of data on male display rate does not improve our ability to predict which males obtain extra-group paternity. The timing of male moult into breeding plumage remains the only predictor of male extra-group reproductive success. Nevertheless, we found that males displayed more to females that were unable to select extra-group mates on the basis of the timing of moult or the onset of display. This raises the possibility that there are circumstances when females use display rate to discriminate between potential extra-group sires. Overall this study supports the theoretical prediction that females are more likely to base their mate choice on reliable indicators of male quality such as fixed morphological traits and displays of endurance, in this case an early moult into breeding plumage and the performance of an elaborate display during the winter, than a flexible behavioural trait such as display rate during the breeding season. Received: 26 January 2000 / Revised: 1 August 2000 / Accepted: 26 August 2000     

Mate sampling behaviour of female pied flycatchers: evidence for active mate choice

Summary This paper presents major new evidence for active mate choice of female pied flycatchers, Ficedula hypoleuca. Fifteen color-ringed females were released into a study area containing 23 unmated males defending one nestbox each. Through intensive surveillance, the behavior of the females was observed during 2 consecutive days. Twenty-two of the males received a total of 131 female visits. Six of the females settled in the study area, and their premating period lasted 1.3–2.5 days. The females were seen searching for mates for at least 6–32 h and were seen visiting at least 1–9 different males. Hence, some of the females rejected males before mating. Nevertheless, the females settled close to the site of release (range: 16–243 m), suggesting that they mated with one of the first males encountered. Females visited males most frequently in the morning, and the diurnal distribution of visits was significantly correlated with male song activity. Offprint requests to: S. Dale     

Female mate selection in the natterjack toad: active choice or passive atraction?

Summary Variation in seasonal mating success among male natterjack toads (Bufo calamita) was influenced by the number of nights that males spent at the pond and by male body size. Large males produced louder and lower frequency calls than small males, and maintained larger acoustic territories. After arriving at the pond, one half of all observed females mated with the first male they encountered. The remainder visited several males before initiating amplexus, but no criteria could be identified that females might have used when deciding whether to accept or reject a male. Movements between several males seem to be best explained by low female responsiveness to male advertisement calls on cold nights which were nonoptimal for oviposition. Females attempted to reject non-calling males both before and after amplexus, but this may be a mechanism to avoid mismating with males of the common toad (Bufo bufo), an explosive breeder that utilised the same pond. In two-choice playback experiments using synthetic advertisement calls, females showed no preference for calls based on their frequency. Females preferred calls of intermediate pulse repetition rate equivalent to those produced by a male at the same body temperature. Pulse rate is thus potentially subject to stabilishing selection and may be an important character for species-recognition. Females preferred fast rather than slow call rates, but only when the alternative rates were extreme. They also preferred calls which they perceived at the highest sound pressure level, but did not discriminate between absolute sound pressure levels of alternative stimuli at different distances. Since females that delay mating and oviposition may suffer predation, it is suggested that female preference for loud, rapidly repeated calls may be adaptive in the sense of minimizing the costs of locating conspecific males, rather than maximizing the probability of obtaining a high quality mate. Competition between males to maintain large acoustic territories and produce calls that can be easily detected by females would seem to be a sufficient mechanism to explain the evolution of the striking calls produced by male natterjacks.     

Close-range acoustic signaling and mate choice in Hawaiian crickets (Gryllidae: Laupala)

Evolution of the mate recognition system (MRS) can play a central role in animal speciation. One dramatic consequence of changes in the MRS is the failure of individuals from divergent lineages to successfully court and mate, thereby reducing gene flow between these groups. Here, we test the role of an acoustic mating signal on mate choice in a Hawaiian cricket genus (Gryllidae: Laupala). Speciation in Laupala is proceeding at an extremely rapid rate, apparently driven by divergence in aspects of the mate recognition system, most conspicuously the pulse rate of male calling song. Previous studies demonstrate that females prefer the pulse rate of a conspecific male’s song when perceived at long range, in laboratory phonotaxis trials. In this study, we examined mate choice in two species that differ dramatically in pulse rate: Laupala paranigra and Laupala kohalensis. We tested the female’s preference in both species for pulse rates at close range, by providing females an opportunity to mate with hybrid males producing a range of intermediate pulse rates. Results of our study demonstrate that while strong behavioral barriers exist between these two species, variation in the pulse rate of male calling song did not predict female mate choice at close range. These results suggest a more complex architecture to mate recognition in Laupala than previously hypothesized.     

Extra-pair paternity in tree swallows: why do females mate with more than one male?

Recent studies of monogamous tree swallows (Tachycineta bicolor) suggest that females may receive some type of genetic benefit from extra-pair fertilizations. In this study we attempted to determine what type of genetic benefits might be gained by females. We compared numerous morphological and behavioral traits (Table 1) of every male nesting on one grid of nest-boxes (n = 23) to determine what male traits were correlated with male success at gaining extra-pair fertilizations. DNA fingerprinting revealed an increase in the level of extra-pair paternity from the previous year (50% of broods contained extra-pair young in 1990 vs. 87% of broods in 1991), but no significant correlates of paternity. We found six extra-pair fathers at seven nests (20 nests had extra-pair young). The traits of these extra-pair males did not differ from those of the males they cuckolded. We discuss several reasons for this lack of difference, but argue that our results are not inconsistent with females choosing extra-pair males to enhance the genotypic quality of their offspring. Despite a complete search of the nest-box grid for extra-pair fathers, we were able to explain the paternity of just 21% (13/63) of all extra-pair young. This suggests that extra-pair fathers were either residents off our study grid or non-territorial floaters. Tree swallows are quite mobile and spend only part of the day at their nest prior to laying. In addition, we rarely see swallows visiting other grids of nest-boxes. Therefore, we suggest that most extra-pair copulations occur at some unknown location, possibly at a feeding or roosting area where females may be able to choose from many more potential extra-pair fathers than at their nest-site.     

Passing the buck: resource defence,lek breeding and mate choice in fallow deer

Summary Lek breeding systems, where males defend small, clustered mating territories, are thought to occur where the distribution of females is heavily clumped but males are unable to defend resources used by females. In this paper, we describe a breeding system in fallow deer where males are able to defend resources used by females but the most successful bucks instead defend small territories on a traditional mating ground; where the lek is sited in an area not heavily used by females at other times of year and is visited primarily by females in or close to oestrus; and where mating success on the lek is related to territory position and to male phenotype but not to the resources available on different lek territories. Comparisons with other ungulates suggest that lek breeding species fall into two groups: those where leks are regularly visited by herds of females many of which are not in oestrus and those, like fallow deer, where leks are visited primarily by oestrous females. In the latter species, it is unlikely that females visit the lek for ecological reasons.