Mating effort and female receptivity : how do male guppies decide when to invest in sex?

Males vary in the degree to which they invest in mating. Several factors can explain this variation, including differences in males’ individual condition and the fact that males allocate their energy depending on the context they face in each mating attempt. Particularly, female quality affects male reproductive success. Here, we studied whether male guppies (Poecilia reticulata) strategically allocated more mating effort, in terms of mating behaviour and male–male competition, when they were matched with a receptive (R) female than a non-receptive one. In accordance with our prediction, we found that males increased their mating behaviour when they were with a receptive female. Even though male guppies can inseminate non-receptive females, we only found high levels of courtship between males that were with a receptive female rather than a non-receptive one. Although there was little affect of female receptivity on male–male competition, we found that males chased and interrupted courtships more with receptive females than with non-receptive females regardless of odour. Finally, we also studied whether the sexual pheromone produced by receptive female guppies is a cue that males use in order to increase their mating effort. We found that males were more attracted to a female when they perceived the sexual pheromone, but only increased their mating and aggressive behaviours when females showed receptive behaviour. This strategic increase in mating effort could result in higher male reproductive success because mating attempts towards receptive females are likely to be less costly and males could have a greater probability of fertilisation.

Inbreeding level does not induce female discrimination between sibs and unrelated males in guppies

Significant empirical evidence has demonstrated the importance of discriminative mate choice as a mechanism to avoid inbreeding. Incestuous mating can be avoided by recognition of kin. The guppy, Poecilia reticulata, is a livebearer with a polygamous mating system and active female choice. Despite potential inbreeding costs in the guppy, Viken et al. (Ethology 112:716–723, 2006) and Pitcher et al. (Genetica 134:137–146, 2008) have found that females do not discriminate between sibs and unrelated males. However, populations experiencing different inbreeding histories can have different levels of inbreeding avoidance, and it is possible that the lack of inbreeding avoidance observed in guppies is a consequence of using outbred fish only. Here we tested the preference of female guppies with different inbreeding coefficients, for olfactory cues of males that were either unrelated but had the same inbreeding coefficient, or were related (i.e. brother) with the same inbreeding coefficient. We found no evidence that female guppies preferred unrelated males with the same inbreeding coefficient. Moreover, inbreeding level did not influence female preference for unrelated males, suggesting that inbreeding history in a population has no influence on female discrimination of unrelated males in guppies.

Females of a viviparous fish (Skiffia multipunctata) reject males with black colouration

This study investigated whether male body colour is a trait upon which females of Skiffia multipunctata, a viviparous fish of the subfamily Goodeinae, base their choice of potential mate. About 60% of the males in the study had black patches on the sides of their bodies and/or dorsal fins. Patches varied in number, size and distribution. Most males (70% of the fish in the study) had diffuse orange colouration on their flanks, mainly on the peduncle. The hypothesis was that, after controlling for differences in body size, females would choose males with more black or orange colouration than males with less exaggerated patches of colour. However, in contrast to this hypothesis, females preferentially approached the males with less black colouration. Since orange colouration did not have a significant effect on female response, and there was no correlation between black and orange colours on the males in the study, females rejected males with more black colouration rather than preferring males with more orange or other visible colours. These findings indicate that sexual selection by female mate choice is not driving black or orange male body colouration in Skiffia multipunctata.

Strategic male signalling effort in a desert-dwelling fish

Males often use elaborate courtship displays to attract females for mating. Much attention, in this regard, has been focused on trying to understand the causes and consequences of signal variation among males. Far less, by contrast, is known about within-individual variation in signal expression and, in particular, the extent to which males may be able to strategically adjust their signalling output to try to maximise their reproductive returns. Here, we experimentally investigated male courtship effort in a fish, the Australian desert goby, Chlamydogobius eremius. When offered a simultaneous choice between a large and a small female, male gobies spent significantly more time associating with, and courting, the former, probably because larger females are also more fecund. Male signalling patterns were also investigated under a sequential choice scenario, with females presented one at a time. When first offered a female, male courtship was not affected by female size. However, males adjusted their courtship effort towards a second female depending on the size of the female encountered previously. In particular, males that were first offered a large female significantly reduced their courtship effort when presented with a subsequent, smaller, female. Our findings suggest that males may be able to respond adaptively to differences in female quality, and strategically adjust their signalling effort accordingly.

Temporal variability in a multicomponent trait : nuptial coloration of female two-spotted gobies

Animals that breed more than once may face different environmental and physiological conditions at each reproductive event. Costs and benefits of sexual ornaments could therefore vary both within and between breeding seasons. Despite this, the ornaments are often assumed to be fixed, and temporal changes in ornamentation have rarely been investigated. Female two-spotted gobies (Gobiusculus flavescens) have colorful orange bellies when sexually mature and nest-holding males prefer females with more colorful bellies. This nuptial coloration is caused both by the carotenoids-rich gonads being directly visible through the skin and by the chromatophore pigmentation of the abdominal skin. Toward the end of the breeding season, males become rare and females become the more competitive sex. We show that female ornamentation of G. flavescens is a complex multicomponent trait and that the separate components, as well as their interactions, are variable. As gonads matured, they became more colorful while the abdominal skin became more transparent, causing more intense belly coloration in sexually mature females. However, coloration varied greatly also among fully mature females, suggesting that it may not only be a signal of readiness to spawn. Indeed, belly coloration predicted gonad carotenoid concentration, but there were several important seasonal differences in color expression. Females sampled toward the end of the breeding season were more colorful. This was due to seasonal increases in both gonad carotenoid concentration and skin coloration. Thus, at a time when competition over males is stronger and the terminal reproductive event approaches, females appear to invest more in signaling.

Does female nuptial coloration reflect egg carotenoids and clutch quality in the Two-Spotted Goby (Gobiusculus flavescens, Gobiidae)?

Summary

1 - Carotenoid-based ornamentation has often been suggested to signal mate quality, and species with such ornaments have frequently been used in studies of sexual selection.

2 - Female Gobiusculus flavescens (Two-Spotted Goby) develop colourful orange bellies during the breeding season. Belly coloration varies among mature females, and previous work has shown that nest-holding males prefer females with more colourful bellies. Because males invest heavily in offspring during incubation, the evolution of this preference can be explained if colourful females provide males with eggs of higher quality.

3 - We tested this hypothesis by allowing males to spawn with ‘colourful’ and ‘drab’ females and comparing parameters including egg carotenoid concentration, clutch size, hatchability and larval viability between groups. We also investigated relationships between egg carotenoid concentration and clutch quality parameters.

4 - Eggs from colourful females had significantly higher concentrations of total carotenoids than drab females, and photographically quantified belly coloration was a good predictor of egg carotenoid concentration.

5 - Colourful females produced slightly larger clutches, but female belly coloration was not related to any measure of clutch quality. In addition, there were no significant relationships between egg carotenoids and clutch quality. Females with high levels of egg carotenoids spawned slightly earlier, however, possibly because they were more ready to spawn or because of male mate choice.

6 - Our results call into question the generality of a causal link between egg carotenoids and offspring quality.

Harem size and oviposition behaviour in a polygynous bark beetle

1. Harem polygyny can have fitness benefits and costs on females. In bark beetles of the genus Ips the latter may include within-harem competition between larvae. However, earlier competition between females for male care and mating opportunities may also influence oviposition behaviour. There has been relatively little investigation into the relationship between harem size and initial egg output. The present study investigated this relationship in the bark beetle Ips grandicollis.
2. The measure of egg output used was the number of eggs in the gallery with the most eggs in each harem. Mean ( ± SE) harem size of 242 observed harems was 3.25 ± 0.10. A curvilinear relationship was found between egg output and harem size, with females in smaller harems (one to four females) laying more eggs with increased harem size. However, females in larger harems (five to seven females) laid fewer eggs as harem size increased. The optimal harem size (in terms of number of eggs laid) was close to four females.
3. We found no evidence from a behavioural assay that females could preferentially choose unmated males over mated males with harems of two females. Additionally, the distribution of harem sizes suggests that females distribute themselves among males randomly.
4. The results suggest that harem size has effects on female reproduction that extend beyond larval competition and influence patterns of oviposition. The mechanism that determines why egg laying is greatest at intermediate levels is unknown. There is no evidence that smaller harems belong to lower quality males, but females may adjust egglaying behaviour in large harems as a result of reduced male attendance or anticipated larval competition.

Maternal stress to partner quality is linked to adaptive offspring sex ratio adjustment

Female birds have been shown to have a remarkable degree of control over the sex ratio of the offspring they produce. However, it remains poorly understood how these skews are achieved. Female condition, and consequent variation in circulating hormones, provides a plausible mechanistic link between offspring sex biases and the environmental and social stresses commonly invoked to explain adaptive sex allocation, such as diet, territory quality, and body condition. However, although experimental studies have shown that female perception of male phenotype alone can lead to sex ratio biases, it is unknown how partner quality influences female physiological state. Using a controlled within-female experimental design where female Gouldian finches (Erythrura gouldiae) bred with both high- and low-quality males, we found that partner quality directly affects female hormonal status and subsequent fitness. When constrained to breeding with low-quality males, females had highly elevated stress responses (corticosterone levels) and produced adaptive male-biased sex ratios, whereas when they bred with high-quality males, females had low corticosterone levels and produced an equal offspring sex ratio. There was no effect of other maternal hormones (e.g., testosterone) or body condition on offspring sex ratios. Female physiological condition during egg production, and variation in circulating hormones in particular, may provide a general mechanistic route for strategic sex allocation in birds.

Response to comment on "Illusions promote mating success in great bowerbirds"

Borgia et al. raise some questions about our recent study showing that great bowerbirds create visual illusions that are used in mate choice. We address them by providing further details about our methods and results. We also provide detailed descriptions of our geometric calculations to address their measurement and analysis questions.

Male great bowerbirds create forced perspective illusions with consistently different individual quality

Males often produce elaborate displays that increase their attractiveness to females, and some species extend their displays to include structures or objects that are not part of their body. Such "extended phenotypes" may communicate information that cannot be transmitted by bodily signals or may provide a more reliable signal than bodily signals. However, it is unclear whether these signals are individually distinct and whether they are consistent over long periods of time. Male bowerbirds construct and decorate bowers that function in mate choice. Bower display courts constructed by male great bowerbirds (Ptilonorhynchus nuchalis) induce a visual illusion known as forced perspective for the female viewing the male's display over the court, and the quality of illusion is associated with mating success. We improved the quality of the forced perspective to determine whether males maintained it at the new higher level, decreased the perspective quality back to its original value, or allowed it to decay at random over time. We found that the original perspective quality was actively recovered to individual original values within 3 d.We measured forced perspective over the course of one breeding season and compared the forced perspective of individual males between two successive breeding seasons. We found that differences in the quality of visual illusion among males were consistent within and between two breeding seasons. This suggests that forced perspective is actively and strongly maintained at a different level by each individual male.

The effects of familiarity and group size on mating preferences in the guppy, Poecilia reticulata

In recent years, it has become evident that frequency dependence in the attractiveness of a particular phenotype to mates can contribute to the maintenance of polymorphism. However, these preferences for rare and unfamiliar male phenotypes have only been demonstrated in small, controlled experiments. Here, we tested the preference for unfamiliar mates in groups of six to 96 individuals over 13 days, in the guppy (Poecilia reticulata). We observed individual behaviour in situ to test whether fish discriminate two unfamiliar individuals among many familiar ones. We found that unfamiliar males and females were preferred over the familiar fishes in all groups and that this effect decayed over time. Increasing group sizes and levels of sexual activity did not hamper the preference for unfamiliar mates, providing further support for the role of frequency dependent mate choice in the maintenance of trait polymorphism in natural populations.

Artificial ornaments manipulate intrinsic male quality in wild-caught zebra finches (Taeniopygia guttata)

The addition of red and green color bands is a commonly used method for manipulating male attractiveness in the zebra finch (Taeniopygia guttata), providing insight into the study of maternal investment and sexual selection. The addition of artificial ornaments has been assumed to manipulate a females’ perception of the male, rather than affecting intrinsic qualities of the male himself. Here, however, we reveal that the artificial band color worn by a male changes his body mass, condition, and courtship display rate. Males wearing red color bands in aviaries prior to mate-choice trials had a significantly higher song rate during trials than those wearing green color bands, alongside a significant increase in mass change and condition. Male song rate was found to significantly correlate with female preference alongside a female preference for red-banded males. However, male song rate in turn increased when female response was positive, suggesting a social feedback between the interacting birds. Our data suggest the presence of socially mediated feedback mechanisms whereby the artificial increase in attractiveness or dominance of a male directly affects other aspects of his attractiveness. Therefore, housing birds in social groups while manipulating attractiveness can directly influence other male qualities and should be accounted for by future studies.

Major histocompatibility complex (MHC) markers in conservation biology

Human impacts through habitat destruction, introduction of invasive species and climate change are increasing the number of species threatened with extinction. Decreases in population size simultaneously lead to reductions in genetic diversity, ultimately reducing the ability of populations to adapt to a changing environment. In this way, loss of genetic polymorphism is linked with extinction risk. Recent advances in sequencing technologies mean that obtaining measures of genetic diversity at functionally important genes is within reach for conservation programs. A key region of the genome that should be targeted for population genetic studies is the Major Histocompatibility Complex (MHC). MHC genes, found in all jawed vertebrates, are the most polymorphic genes in vertebrate genomes. They play key roles in immune function via immune-recognition and -surveillance and host-parasite interaction. Therefore, measuring levels of polymorphism at these genes can provide indirect measures of the immunological fitness of populations. The MHC has also been linked with mate-choice and pregnancy outcomes and has application for improving mating success in captive breeding programs. The recent discovery that genetic diversity at MHC genes may protect against the spread of contagious cancers provides an added impetus for managing and protecting MHC diversity in wild populations. Here we review the field and focus on the successful applications of MHC-typing for conservation management. We emphasize the importance of using MHC markers when planning and executing wildlife rescue and conservation programs but stress that this should not be done to the detriment of genome-wide diversity.

Visual effects in great bowerbird sexual displays and their implications for signal design

It is often assumed that the primary purpose of a male's sexual display is to provide information about quality, or to strongly stimulate prospective mates, but other functions of courtship displays have been relatively neglected. Male great bowerbirds (Ptilonorhynchus nuchalis) construct bowers that exploit the female's predictable field of view (FOV) during courtship displays by creating forced perspective illusions, and the quality of illusion is a good predictor of mating success. Here, we present and discuss two additional components of male courtship displays that use the female's predetermined viewpoint: (i) the rapid and diverse flashing of coloured objects within her FOV and (ii) chromatic adaptation of the female's eyes that alters her perception of the colour of the displayed objects. Neither is directly related to mating success, but both are likely to increase signal efficacy, and may also be associated with attracting and holding the female's attention. Signal efficacy is constrained by trade-offs between the signal components; there are both positive and negative interactions within multicomponent signals. Important signal components may have a threshold effect on fitness rather than the often assumed linear relationship.

Artificial selection for food colour preferences

Colour is an important factor in food detection and acquisition by animals using visually based foraging. Colour can be used to identify the suitability of a food source or improve the efficiency of food detection, and can even be linked to mate choice. Food colour preferences are known to exist, but whether these preferences are heritable and how these preferences evolve is unknown. Using the freshwater fish Poecilia reticulata, we artificially selected for chase behaviour towards two different-coloured moving stimuli: red and blue spots. A response to selection was only seen for chase behaviours towards the red, with realized heritabilities ranging from 0.25 to 0.30. Despite intense selection, no significant chase response was recorded for the blue-selected lines. This lack of response may be due to the motion-detection mechanism in the guppy visual system and may have novel implications for the evolvability of responses to colour-related signals. The behavioural response to several colours after five generations of selection suggests that the colour opponency system of the fish may regulate the response to selection.