Cues In Mate Choice Research Articles

Male gopher tortoise (Gopherus polyphemus) concentration-dependent social responses to diluted mental gland pheromones

In complex terrestrial environments, chemical signals can be the most important sensory modality for locating conspecifics for potential mating opportunities, especially in spatially segregated populations or habitats. Organisms must evolve chemical signals to maximize the efficacy of conveying information, particularly in creating trails or mate-choice cues. Long-distance transmission of chemical signals may be an increasingly important management concern for small and fractured populations or potentially threatened species, such as gopher tortoises in the southeastern U.S. Mental gland secretions have been shown to have pheromonal function in gopher tortoises, suggesting a potential role as trail or marking pheromones, allowing males to track females or other males to find females. In this study, male gopher tortoises were given paired presentations of a negative control (distilled water) with serial dilutions (1:4, 1:20, 1:100, and 1:500) of male mental gland secretions. Male tortoises were able to discern treatment differences up to 1:20 diluted secretions, responding with an array of social behaviors (e.g. for the 1:20 dilution trial, carapace alignment and head bobbing occurred more frequently for the mental gland secretion relative to the control; p < 0.01). Multivariate principal components analysis yielded PC1 (including, approach, carapace alignment, head bobbing, tasting air, sniffing, and doubleback) that differed by treatment (p = 0.0007) and also was higher for the 1:20 diluted presentation relative to the 1:500 diluted presentation (p = 0.04). This study provides insight into gopher tortoise ecology, mate-choice, and the utility of environmentally diluted mental gland secretions in the external environment when seeking mating opportunities.

Conspecific olfactory preferences and interspecific divergence in odor cues in a chickadee hybrid zone.

Understanding how mating cues promote reproductive isolation upon secondary contact is important in describing the speciation process in animals. Divergent chemical cues have been shown to act in reproductive isolation across many animal taxa. However, such cues have been overlooked in avian speciation, particularly in passerines, in favor of more traditional signals such as song and plumage. Here, we aim to test the potential for odor to act as a mate choice cue, and therefore contribute to premating reproductive isolation between the black‐capped (Poecile atricapillus) and Carolina chickadee (P. carolinensis) in eastern Pennsylvania hybrid zone populations. Using gas chromatography–mass spectrometry, we document significant species differences in uropygial gland oil chemistry, especially in the ratio of ester to nonester compounds. We also show significant preferences for conspecific over heterospecific odor cues in wild chickadees using a Y‐maze design. Our results suggest that odor may be an overlooked but important mating cue in these chickadees, potentially promoting premating reproductive isolation. We further discuss several promising avenues for future research in songbird olfactory communication and speciation.

The endocrine disruptor, 17α-ethinyl estradiol, alters male mate choice in a freshwater fish

Among the handful of studies on the behavioural effects of endocrine disrupting chemicals (EDCs), only a few have set out to disentangle the mechanisms underpinning behavioural changes. In fish, previous studies have shown that both visual and chemical cues play an important role in mate choice. As such, contaminant-induced changes in either transmission or perception of mate choice cues could have direct implications for individual’s fitness. One widespread contaminant of environmental concern is 17α-ethinyl estradiol (EE2), a synthetic estrogen used in the contraceptive pill. Here, we investigated the impacts of EE2 exposure (28 days; measured concentration 14 ng/L) on visual and chemical communication in wild guppies (Poecilia reticulata). Using a standard dichotomous mate choice assay, we first gave individual males (either control or EE2-exposed) the opportunity to court two size-matched females (one control and one EE2-exposed) using only visual cues. We then introduced chemical cues of females (control and EE2-exposed) to the trial tank. We found that there was no significant effect of EE2-treatment on total time males spent associating with the females, when given only visual cues. There was, however, a significant effect on male courtship behaviour, with both control and EE2-exposed males spending more time performing ‘sigmoid’ displays towards the visual cues of control females compared to EE2-exposed females. When males were presented with both visual and chemical female cues simultaneously, we found that males spent more time courting control females that were paired with EE2-chemical cues. Not only does our study uncover a previously unknown behavioural impact of EE2-exposure on chemical cues, but demonstrates that EE2-exposure can exert complex effects on visual and chemical communication in a mate choice context. Finally, we contribute to the discussion of intraspecific variability by providing data on the potential trade-offs underpinning contaminant-induced behavioural changes.

Behaviour of Arctic charr Salvelinus alpinus during an induced mating season in captivity: how male relative size influences male behavioural investment and female preference over time.

The behaviour of sexually mature Arctic charr Salvelinus alpinus specimens (fifth farm generation) was observed in captivity for four consecutive days. Only agonistic interactions between males of different size were facilitated on the first 2 days, while both agonistic and courtship interactions were possible from the third day up to the end of the experiment. The reliability of behavioural analysis was assessed in order to reduce the possibility of observer errors within the generated datasets. The behavioural investment of big males, small males and females was analysed using general linear models (two-way repeated measures ANOVAs with time and male size as factors). A peak in the agonistic interactions between males occurred during the first day of interactions, where the agonistic investment of big males was significantly higher than that of small males. This resulted in an increased investment in submissive behaviour by the small males, who consistently performed submissive behaviours from the second day of interactions up to the end of the trial. Big males were found to invest significantly more than small males in courtship behaviours for the duration of the trial. Even though females performed inter-sexual behaviours towards both big and small males for the entire observation period, female interaction rate towards big males was higher than towards small males. This study suggests that both male investment in mating behaviour and female preference might be related to male characteristics such as body length and that S. alpinus behavioural patterns and mate choice cues might be strongly context-related and characterized by high levels of behavioural plasticity (i.e. presence-absence of certain behavioural units or potential reversal of a mate choice cue) within the same species. Finally, in light of this, some conservation measures are discussed. In particular, effective management plans should take into account the high level of behavioural plasticity likely to be occurring in this species.

Environmental Change and Extended Phenotypes: Does Eutrophication Influence Nest Building in Sticklebacks?

AbstractMany species use extended phenotypes, such as purpose‐built nests, to increase their reproductive success. These traits have to be adjusted to local environmental conditions to maximize fitness. An important question is whether species are able to adjust their extended phenotypes to human‐induced rapid environmental changes. We investigated whether populations of threespine stickleback, Gasterosteus aculeatus, exposed to different degrees of human‐induced eutrophication during the last decades, have differentiated phenotypically in their nest‐building behaviour. Stickleback males build nests that they use both in mate attraction and for offspring protection and whose characteristics vary with environmental conditions. We allowed males from parallel pairs of mildly and severely eutrophied habitats to build nests under standardized conditions in the laboratory. We recorded the time it took the males to build a nest, the size and neatness of the completed nest and the use of nest ornaments. We found eutrophication at the site of capture to influence nest‐building time – males from eutrophied habitats built faster. However, eutrophication did not alter nest structure or the use of nest ornaments. This is probably because the nests are concealed in vegetation or under stones and females cannot evaluate them before they have followed the male to the nest, and predators cannot detect them before close to the nest. Thus, reduced long‐range visibility does not influence the use of nests as mate choice cues or for offspring protection. This contrasts with a recorded effect of eutrophication on courtship behaviour, whose efficiency depends on long‐range visibility. This suggests that traits are adjusted to eutrophication depending on the influence of eutrophication on the function of the traits.

Female preference for blue in Japan blue guppies (Poecilia reticulata)

Guppies (Poecilia reticulata) are widely used as a model species in mate choice studies. Although native to South America, guppies have been introduced to natural water bodies in disparate regions of the globe. Here, for the first time, we examine guppies from one such introduced population in Japan where males have evolved a predominantly blue color pattern. Previous studies of wild-type guppies have shown blue to play a relatively minor role in the mate choice decisions of females compared to other traits, such as orange, and the importance of blue is not universally supported by all studies. The Japanese population therefore presents an ideal opportunity to re-examine the potential significance of blue as a mate choice cue in guppies. Mate choice experiments, in which female Japan blue guppies were given a choice between pairs of males that differed in their area of blue coloration but were matched for other traits, revealed that females prefer males with proportionately larger amounts of blue in their color patterns. We discuss possible factors, including sexual and ecological selection, which may have led to the evolution of unusually large areas of blue at the expense of other colors in Japan blue guppies. However, further studies are needed to distinguish between these scenarios.

Repeatability of nest size choice and nest building in sand gobies

To be useful as mate choice cues, behavioural traits have to be performed consistently within individuals. This may also be true for nest construction, which, in addition to influencing offspring survival, can also function as an extended phenotype of the builder. We tested whether choice of a nesting resource and subsequent nest-building performance are repeatable traits in the sand goby, Pomatoschistus minutus , a small marine fish with paternal egg care and female mating preferences that are influenced by male nest-building behaviour. When given a choice between three different-sized nesting resources (flowerpots), males, on average, preferred medium-sized nesting resources, with larger males preferring larger nests than smaller individuals. At the individual level, the choice of nesting resources was so variable between consecutive trials that choice behaviour was not repeatable. Furthermore, nest building, measured as the amount of sand piled on top of the nesting resource, was highly repeatable when males were free to choose their nest, but had only a low repeatability when males had just a single option. In neither case was the size of the nest entrance repeatable between consecutive rounds of nest building. These results highlight the context-dependent signal value of extended phenotypes. In particular, reliability of nest-building behaviour as a signal seems to be influenced by the male's opportunity to choose the object it uses for nesting. ► Nest characteristics can have a major effect on parents' reproductive success. ► We assessed consistency of nest resource choice and nest building in sand gobies. ► Larger males chose larger nests but choices were variable within individuals. ► Repeatability of nest building varied between contexts and nest characters. ► Hence, some but not all aspects of nest building can function as reliable signals.

Diet and mate choice cues affect central catecholamine levels in a species with condition-dependent mate choice

Diet and mate choice cues affect central catecholamine levels in a species with condition-dependent mate choice

Queuing in space and time reduces the lek paradox on an antelope lek

Lek systems, where females often use centrality to assess male quality, highlight a general paradox in evolutionary biology: how can female preferences for males providing good genes persist when consequential strong directional selection is predicted to deplete additive genetic variance in male quality and thereby obliterate benefits of choosiness? An explanation contributing to the resolution of this lek paradox may be that genetic variance is retained when an indirect mate choice cue, such as centrality on a lek, is an imperfect indicator of male genetic quality. Here I investigate whether the presence of alternative male mating tactics limits the reliability of centrality as a quality indicator in lek-breeding topi antelopes. Whereas males establishing territories directly on the central lek were relatively large, smaller peripheral males regularly shifted their territories centripetally and in this way also occasionally obtained central territories. By such opportunistic queuing, small males could increase their mating success drastically; however, their territorial tenure in the lek centre was relatively short, consistent with moderate competitive ability. These results suggest that male topi antelopes can obtain central lek territories through alternative mating tactics, providing scope for variance in male quality on the central lek. In a separate finding, the mating success of central males was found to increase during territorial tenure, independent of estimated age. The demonstration of queuing in both space and time on a mammalian lek highlights the importance of considering male tactical dynamics over time in order to avoid an inflated appearance of the lek paradox.

CONVERGENT EVOLUTION OF RED CAROTENOID COLORATION IN WIDOWBIRDS AND BISHOPS (EUPLECTES SPP.)

Avian carotenoid-based signals are classic examples of sexually selected, condition-dependent threat displays or mate choice cues. In many species, male dominance or mating success is associated with redder (i.e., longer wavelength) color hues, suggesting that red colors are either more efficient or more reliable signals than yellow colors. Few studies, however, have investigated selection for redness in a macroevolutionary context. Here, we phylogenetically reconstruct the evolution of carotenoid coloration in the African widowbirds and bishops (Euplectes spp.), for which agonistic selection for redder hues, as well as pigmentary mechanisms, is well documented. Using reflectance spectrometry for objective color quantification, and accounting for phylogenetic uncertainty, we find that yellow plumage color is a retained ancestral state in Euplectes, and that red color hues have convergently evolved two or three times. Results are discussed in relation to a known diversity in pigment mechanisms, supporting independent origins of red color, and suggesting that agonistic selection and physiological constraints have interacted to generate color diversity in Euplectes.

Foxn1 Gene Knockout Suppresses Sexual Attractiveness and Pheromonal Components of Male Urine in Inbred Mice

The immunocompetence handicap hypothesis (ICHH) posits that females prefer signals emitted by immunocompetent males over immunocompromised males and that these signals are honest. However, mechanisms of mate choice under an ICHH model may be impacted by levels of genetic variation (inbred animals vs. outbred animals). Here, we conducted 2-choice female preference experiments and chemical analyses of male urine in inbred BALB/c and outbred CD-1 mice, both of which have immunocompromised nude (nu) strains resulting from a Foxn1 gene knockout. We found that inbred BALB/c females but not outbred CD-1 females preferred the urine of healthy males over that of immunocompromised males despite measured differences in the qualities of their urine. There was a clear increase in female-attracting pheromones (such as farnesenes) in the preputial glands and urine metabolites in healthy BALB/c males but no such difference between CD-1 and CD-1 nu males. Therefore, CD-1 male urine failed to provide an honest mate-choice cue for females. Our results suggest that deleterious traits associated with male odor in mice might be jointly affected by the level of inbreeding and immunodeficiency caused by a single-gene knockout.

Distinguishing between male and territory quality: females choose multiple traits in the pied flycatcher

To understand how sexual selection works, it is important to distinguish between the mechanisms underlying mating success. One of the basic questions is to differentiate between the importance of territory-related resources (gained through male–male competition) and male quality in female choice. Few studies, however, have tried to separate these two often intercorrelated variables. We randomized territory quality among male pied flycatchers, Ficedula hypoleuca, and studied which male traits were associated with their success in female mate choice. Females appeared to choose multiple male traits in the wild when the males were not allowed to choose territories before female choice for males. Males with a long tarsus, large white wing patch and versatile song were favoured by females. In addition, the contrast of ultraviolet (UV) reflectance in the white wing patch relative to its background, that is, the dorsal brown-black coloration of the males, appeared to be an important mate choice cue. The UV reflectance had a stronger effect on pairing success in dark males than in brown ones. An experimental manipulation of the UV reflectance revealed that the UV coloration of the males appeared to be used in female choice early but not late in the pairing season, which suggests time-dependent plasticity in female choice. Our study thus exemplifies the complexity of mate choice; it is both temporally constrained and dependent on multiple ornaments.

Variance in reproductive success and the opportunity for selection in a serially monogamous species: simulations of the mating system of Tropheus (Teleostei: Cichlidae)

Sexual selection is believed to play a major role in speciation processes of cichlid fishes in the East African Great Lakes, in particular Lakes Malawi and Victoria, by driving diversification in male nuptial coloration. In Lake Tanganyika, a high rate of color pattern diversification is found in the genus Tropheus, where more than 100, mostly allopatric, color morphs have been described. Whether color pattern differentiation in Tropheus could follow from sexual selection as well, has not yet been conclusively shown. Unlike typical sexually selected species, Tropheus are sexually monomorphic, establish temporary pair bonds and spawn monogamously. Variance in mating success among individuals would still allow for sexual selection, but due to their high population census sizes, parentage data from natural populations are difficult to obtain. Simulations designed according to existing data on mating behavior in Tropheus suggested that variance in male reproductive success can be substantial and lead to levels of opportunity for selection, which are similar to values estimated, for example, from natural populations of sexually dimorphic songbirds. Variance in male success was mostly affected by the way females perceived and reacted to differences between males, and to a lesser extent by the duration of components of the reproductive cycles of males and females. These results indicate that future work on the importance of sexual selection in Tropheus should concentrate on mate choice cues and female mate choice behavior, but does not depend critically on the acquisition of more detailed life history data.

Extra-pair paternity in the socially monogamous Sedge Warbler Actocephalus schoenobaenus as revealed by multilocus DNA fingerprinting

A marked population of Sedge Warblers Acrocephalus schoenobaenus was studied from 1993-95, the reproductive success of pairs was monitored and blood samples collected for DNA profiling. Measures of male physical and behavioural traits were also made, including song repertoire size, the amount of time spent singing and song-flighting, as well as territory quality. Although the Sedge Warbler is generally considered to be monogamous, social polygyny occurred in both 1994 and 1995, giving an overall rate for the two years of 7.7% of males. The overall rate of extra-pair paternity in the population was found to be 8.4% of offspring, with 34.4% of broods containing one or more extra-pair young. No incidences of intra-specific brood parasitism (egg dumping) were identified. Cuckolded males were compared with other males, but no significant differences were identified for any of the physical, behavioural or territorial measures. In particular, there was no evidence that previously detected mate choice cues are related d to patterns of paternity within the population, and hence no evidence that such cues indicate genetic benefits to females. It therefore seems likely that repertoire size reflects male phenotypic quality in this species.

Bacular variation and allometry in the western martenMartes caurina

Many sexually-selected structures are variable and positively allometric relative to body size. For the western martenMartes caurina Merriam, 1890 from Vancouver Island, British Columbia, we investigated variation in the baculum compared with other bones and allometry of bacular to body size. Carcass length did not differ, and humeral and mandibular lengths differed little (< 1 and 2%, respectively), between age groupings < 1 and ≥ 1 yr old. In contrast, bacular length increased by 16%, and thickness by 29% (mid shaft) and 86% (basal) between those groupings, and thickness and mass continued to grow after the second year of life. Controlling for body size, bacular size varied more than humeral or mandibular size (CV for linear variables ∼4–8% for baculum, ∼2% for humerus or mandible). Some positive static allometry of bacular size to body size was found, but correlations between bacular and body size were weak (r=0.3–0.4). So penile size as related to bacular size could be a reliable but imprecise quality indicator during copulation. Weak polygamy (serial promiscuity), complex copulatory mechanisms, and high energetic costs of reproduction, likely select for multiple cues in mate-choice by females, not just penile cues affected by bacular size or shape.

UVB-Based Mate-Choice Cues Used by Females of the Jumping Spider Phintella vittata

Although there are numerous examples of animals having photoreceptors sensitive to UVA (315-400 nm) [1] and relying on UVA-based mate-choice cues [2-5], here we provide the first evidence of an animal using UVB (280-315 nm) for intraspecific communication. An earlier study showed that Phintella vittata, a jumping spider (Salticidae) from China, reflects UVB [6]. By performing six series of binary mate-choice experiments in which we varied lighting conditions with filters (UVB+ [no filter] versus UVB-, UVB+ versus ND1, UVB+ versus ND2, UVB- versus ND1, UVB- versus ND2, and UVB- versus UVA-), we show that significantly more UVB + males than UVB- males are chosen by females as preferred mates. Female preference for UVB-reflective males is not affected by differences in brightness or by UVA.

Female preferences for long tails constrained by species recognition in short-tailed red bishops

Sexual selection and species recognition both play important roles in mate choice. Typically, females use the relative expression of male sexual traits to select high-quality or attractive mates (sexual selection) of the same species (species recognition). However, when the variation in male trait expression of both conspecifics and heterospecifics overlaps, females potentially face a conflict between sexual selection and mate recognition. Among the highly polygynous and closely related African Euplectes species (widowbirds and bishops), females show a general and open-ended mate preference for extreme male tail length (even in relatively short-tailed species). To evaluate the relative strength and interaction of directional versus stabilizing selection pressures on tail length, we experimentally examined female mating preferences in the red bishop (Euplectes orix), a short-tailed (4 cm) species sympatric with longer tailed widowbirds (tails 7–50 cm). In standardized mate-choice experiments, females preferred naturally long-tailed males (5 cm), were indifferent to controls (4 cm), but discriminated against short-tailed (3 cm) and supernormal-tailed (8 cm) males. Although the naturally small variation in tail length (5%) is unlikely to function as a primary mate-choice cue, these results suggest a generalized female bias for longer tails (within the natural range). However, directional preferences for longer tails may be constrained by selection pressures to avoid heterospecific mating with the closely related and sympatric longer tailed widowbirds.

Neural orchestration of mate-choice plasticity in songbirds

Females may choose between prospective mates based on signals that reflect male quality. In songbirds, variation in male song can be such a signal. Females can adjust their choosiness according to the prevalence of preferred song, presumably because environmental variation can influence the availability of preferred phenotypes. Studies using induction of the immediate early gene ZENK (also called zif-268, egr-1, NGFI-A, and Krox-24) as an indicator of neuronal activity have revealed that the caudomedial mesopallium (CMM) and caudomedial nidopallium (NCM) of the female auditory forebrain are sensitive to song quality and respond proportionally to the strength of the female’s choosiness. In European starlings (Sturnus vulgaris), long songs are preferred by females and induce higher ZENK expression in the CMM and NCM compared to short songs. Experimentally reducing the perceived prevalence of long songs in the environment reduces this forebrain sensitivity to song length, raising the possibility that the songbird auditory forebrain integrates information about the social environment that enables the female to adjust her choosiness according to the availability of preferred phenotypes. In some songbird species, the noradrenergic system modulates mate-choice behavior, modulates song-induced auditory forebrain activity, and itself is modulated by the prevailing song environment, suggesting a possible role for this system in mediating the effects of social environment on forebrain and behavioral sensitivity to mate-choice cues. The presence of such a system would seem beneficial when the availability of preferred mates varies.

Absence of status signalling by structurally based ultraviolet plumage in wintering blue tits (Cyanistes caeruleus)

Structurally based ultraviolet (UV)-reflective plumage parts can be important cues in mate choice. However, it remains largely unknown if UV plumage variation can also function as a signal of social status during competitive interactions. In blue tits (Cyanistes caeruleus), the UV-reflective crown plumage functions as a female mate choice cue that probably indicates male quality, as males with higher UV reflectance have been shown to have better chances of over-winter survival. Possibly, the UV crown plumage acts as a status signal in the competition over scarce food sources during winter. To test this idea, we related dominance of individuals at an artificial food source during adverse winter conditions to spectrophotometric measurements of their crown plumage. However, while controlling for the confounding effects of sex, age, and distance from territory, we found no significant effect of crown UV reflectance on dominance. Consistent with this result, we also found no relation between crown UV reflectance and over-winter survival. We conclude that the structurally based UV reflectance of the blue tit crown feathers plays little role in competition between individuals during winter despite its importance as a cue in mate choice.

Mate preference for multiple cues: interplay between male and nest size in the sand goby, Pomatoschistus minutus

Female mating preferences are often based on more than one cue. In empirical studies, however, different mate choice cues are typically treated separately ignoring their possible interactions. In the current work, we studied how male body size and size of the male’s nest jointly affect mate preferences of female sand gobies, Pomatoschistus minutus. The females were given a binary choice between males that differed either in body size or size of their nest or both. We found that neither body size nor size of the nest alone affected male attractiveness, but together these 2 cues had a significant effect. Specifically, large males were more popular among females when they had a large nest than when they occupied a small nest. The results suggest that if interaction effects between multiple mate choice cues are not considered, there is a danger of ignoring or underestimating the importance of these cues in sexual selection by female choice. Key words: mate choice, multiple cues, nest size, Pomatoschistus minutus, sexual selection. [Behav Ecol]