Male-male competition ensures honest signaling of male parental ability in the three-spined stickleback (Gasterosteus aculeatus)

The importance of socially imposed costs for the evolution and maintenance of honest sexual signals has received less attention than other costs. Here I show that male-male competition can increase the honesty of sexual signaling in relation to male parental ability in a species with flexible signaling. When four three-spined stickleback (Gasterosteus aculeatus) males were allowed to court a female first separately and then in competition, red nuptial coloration under competition reflected male parental ability more accurately than red coloration when separated. Parental ability was determined as the ability of the male to raise a clutch of eggs to the hatching stage under interaction with other breeding and non-breeding males. The increased honesty under competition was probably due to subordinate males of poor parental ability decreasing their color expression under interaction to reduce the risk of fights with superior males. However, socially imposed costs of signaling were probably not the main factors maintaining honest signaling, as red coloration reflected male parental ability also in the absence of competition, although less accurately. Nevertheless, the small-scale differences that male-male competition induced can significantly facilitate adaptive female choice and have large impacts on sexual selection. Received: 7 July 2000 / Revised: 31 August 2000 / Accepted: 4 September 2000     

UV wavelengths make female three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>) more attractive for males

Numerous fishes possess UV vision and show UV patterns, which often play a role in social communication, especially during courtship. UV light is scattered strongly in water and thus might be used for intra-specific close-range communication without being detected by predators. In addition to the red-belly colouration and blue-coloured iris, male three-spined sticklebacks possess UV reflectance on their skin, and females prefer males presented with UV light rather than without. To investigate whether UV also influences male visual preference for females in this species, we used a dichotomous mate choice design in which one female could be viewed by a male in two visual conditions. Courting male sticklebacks preferred females that were presented in full-spectrum conditions including UV to the same females presented in conditions lacking this light component. Furthermore, control trials with neutral-density filters indicated that male preference in the UV treatment was not affected by a difference in achromatic brightness between the UV+ and UV− stimuli. Reflectance measurements of gravid females suggest an enhanced UV contrast between the dark bar pattern, which is characteristic of gravid females, and silvery body parts.     

The artistic three-spined stickleback (<Emphasis Type="Italic">Gasterosteous aculeatus</Emphasis>)

We investigated whether female three-spined sticklebacks ( Gasterosteus aculeatus) are more attracted to a male whose nest contains colourful artificial material than to a nest that only contains algae. The purpose was to examine whether nest characters are of importance for female choice in the three-spined stickleback. Most studies on female preference in this species have focused on male morphological traits. In our study, on a marine population of three-spined stickleback on the West coast of Sweden, we found that males marked their nests' entrance with a deviant colour of algae — an apparent decoration. Moreover, males also decorated their nests with shiny and colourful foil sticks and spangles when provided with such, thereby apparently reducing the nest camouflage. In a mate choice experiment, females were more attracted to males with nests containing sticks and spangles than to males with undecorated nests. Nest decoration may be important for the evolution of paternal care in this species: if males advertise their paternal skills by ornamenting their nest they will receive more matings than males with dull nests.     

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.     

Territory quality affects female preference in a Lake Victoria cichlid fish

Mate preferences on male colour have been implicated in generating and maintaining species diversity among haplochromine cichlid fish. Their lek-like mating system suggests that not only male colour but also territory quality is instrumental in mate choice. We assessed the relative importance of territory quality and male colour in mate choice by testing whether territory quality can override the female preference for males of her own colour in the Lake Victoria cichlid genus Pundamilia. First, we showed in experimental groups that the dominant male preferentially monopolised a large tube relative to a small tube. The situation mimics quality difference in rocky crevices that serves as a focal point for male courtship display. Second, in mate-choice tests, Pundamilia nyererei females were allowed to choose between closely related P. nyererei and P. pundamilia males; these species differ strikingly in male nuptial coloration, but little else. We gave either both males the same small tube or one of them a large tube. The preference of P. nyererei females for P. nyererei males in the control situation (where both males had a small tube) was significantly diminished in favour of P. pundamilia males when the latter had the large tube. The results provide experimental evidence that differences in territory quality can override the female preference for males of her own colour. This finding is critical for a recent hypothesis proposing that male competition for mating territories can facilitate the process of sympatric speciation by sexual selection.     

Polygyny in the red-winged blackbird: do females prefer monogamy or polygamy?

Five hypotheses have been proposed to explain polygyny in the red-winged blackbird (Agelaius phoeniceus). We categorized the hypotheses into three groups based on female preference for unmated versus monogamously mated males: (1) the “polygyny threshold” model, “sexy son” hypothesis and the “asynchronous settlement” model, which assume that females prefer unmated males to mated males on breeding situations of homogeneous quality; (2) the “neutral mate choice” hypothesis, which assumes that females have no preference; and (3) the “cooperative female choice” model, which assumes that females prefer monogamously mated males to unmated males. We tested the direction of female preference in two field experiments. In both experiments, newly settling females were given a choice of two adjacent territories, one defended by an unmated male and the other by a monogamously mated male. Male mating status was randomized with respect to the variation in territory quality and male quality. Early in the breeding season, significantly more females settled with the unmated males than with the mated males. Although more females settled with the unmated males than with the mated males late in the breeding season, the difference was no longer significant. Female settlement late in the season appeared to be related to the tenure of the resident females: the new females avoided territories where the resident females were in early stages of their nesting, but settled on territories where the resident females were in late stages. The pattern of female settlement shows that females prefer unmated males to mated males. The preference is consistent with the polygyny threshold model, sexy son hypothesis and the asynchronous settlement model, and inconsistent with the neutral mate choice hypothesis and the cooperative female choice model. For this reason, the latter two hypotheses are unlikely to explain the occurrence of polygyny in our population of red-winged blackbirds. Received: 1 December 1994 / Accepted after revision: 28 October 1995     

Female European green lizards (Lacerta viridis) prefer males with high ultraviolet throat reflectance

The role of ultraviolet (UV) signals in intraspecific communication has been identified in a number of vertebrate taxa. In lizards, the signalling role of UV has only been shown in male–male competition and male mate choice. Here, we investigated whether male UV colour can be a basis of female association preference in European green lizards (Lacerta viridis), a species where males develop blue nuptial throat colouration with high UV reflectance. We experimentally manipulated the UV colour of male pairs, where the members of the pair did not differ significantly in body length, body weight, head size, throat UV chroma and brightness or throat blue chroma and brightness measured prior to colour manipulation. By providing these pairs of males to females (only visual stimuli could be perceived by the females), we assessed the role of UV in female association preference irrespective of other potentially important visual traits. We found that unmated but receptive females preferred males of higher UV reflectance. Our results show for the first time that UV colour can be an important male signal in female preference in reptiles.     

Bushcricket song as a clue for spermatophore size?

Bushcricket males of Poecilimon zimmeri transfer large and protein-rich spermatophores during mating, which females directly ingest. There is correlational evidence that heavier males transfer larger nuptial gifts. In no-choice mating trials, females mated randomly with respect to male’s body weight. In contrast, in two-choice mating trials, female bushcrickets exhibit clear choice for the heavier male. This heavier male advantage was also found in pre-mating choice during phonotaxis. With manipulated mute males, females mated at random with regard to body weight of the competitors. The number of physical encounters between a female and males was low in all tests with a single male (no choice) and greater in choice-tests with two competing males. The latencies to mate also differed significantly between treatments. The time mating pairs spent in precopula was short in experiments where the males could hear rivals and significantly longer in all other tests using either a single male or mute males. Thus, acoustic signalling in male bushcrickets seems to signal male body weight. A preference for heavier males may reflect a female’s preference for a larger spermatophore and therefore a greater direct benefit.     

Testosterone is involved in acquisition and maintenance of sexually selected male plumage in superb fairy-wrens, Malurus cyaneus

Testosterone has been proposed as a physiological link between the level of sexual signalling and male condition. Bright plumage is one of the most noticeable sexual signals and is often used by females as a basis for mate choice. Yet bright male plumage is not necessarily testosterone dependent. We investigated the role of testosterone in the moult into seasonal nuptial plumage in male superb fairy-wrens. Early pre-nuptial moult is under intense intersexual selection and males can acquire the bright plumage any time between autumn and the next spring. Testosterone was always undetectable or very low in males in dull eclipse plumage. During the pre-nuptial moult, both the number of males with detectable testosterone and average testosterone levels increased sharply. High testosterone was more correlated with nuptial plumage than with presence of the cloacal protuberance (indicative of sperm storage). Subcutaneous testosterone implants always induced the pre-nuptial moult within 2–3 weeks after implantation, even well outside the natural time range of moulting. Moreover, removal of the implants before the nuptial plumage was completed, arrested the moult process. The evidence suggests that development of the nuptial plumage is testosterone dependent, although we cannot exclude that testosterone exerts its action after conversion to a metabolite such as oestrogen. Once the nuptial plumage was completed, all males maintained substantially elevated testosterone, sometimes months before the onset of breeding. These high levels could be necessary to maintain the plumage, and/or are involved in courtship displays. The results are discussed with respect to potential costs involved in acquiring and maintaining the nuptial plumage. Received: 17 January 2000 / Received in revised form: 24 February 2000 / Accepted: 25 February 2000     

The influence of potential reproductive rate and variation in mate quality on male and female choosiness in the sand goby, Pomatoschistus minutus

Recent models of choosiness in mate choice have identified two particularly important factors: the potential reproductive rate (PRR) of the choosing sex relative to that of the chosen sex, and the variation in quality of potential mates. This experimental study tested how these factors affected choosiness in male and female sand gobies, Pomatoschistus minutus. We manipulated relative PRR by means of water temperature, and mate quality by means of body length. The choosing male or female was offered a choice between two mates with either a small or a large difference in body length representing a small or a large variation in mate quality. Choosiness was measured as (1) preference for the larger mate, and (2) as whether or not spawning occurred with the smaller mate, while the larger mate was visible but screened off. We found that females preferred large males, and that their level of choosiness was affected by variation in male quality, but not by their own relative PRR. Males, on the other hand, seemed unselective in all treatments and were in general more likely than females to spawn with their provided partner. This suggests that in the sand goby, variation in male mate quality has a greater influence than relative PRR on facultative changes in female choosiness. However, a general difference in PRR between males and females may be one important factor explaining the observed sex difference in choosiness. Received: 17 April 2000 / Revised: 24 June 2000 / Accepted: 17 July 2000     

Does female plumage coloration signal parental quality? A male removal experiment with the bluethroat (Luscinia s. svecica)

Females in several sexually dimorphic species with conventional sex roles possess ornamental traits that resemble those found in males. The evolution of such traits, however, is still poorly understood. Bluethroats (Luscinia s. svecica) are socially monogamous, sexually dichromatic passerine birds, in which female throat patch coloration varies from near absence to near full expression of male-like coloration. A recent study, demonstrating that male bluethroats prefer colourful females, suggests that female coloration is subject to sexual selection through male choice. However, the benefits males may gain from mating with colourful females have not yet been identified. In this study we tested the hypothesis that female coloration signals parental quality (the good-parent hypothesis). During the course of the same day, we recorded female care both in the presence and the absence of the male mate. The latter was done to eliminate the confounding effect of variable male care by removing the male temporarily. Female coloration did not correlate with female feeding rates either in the presence or in the absence of the male. Female feeding rates in the absence and the presence of the male were positively, although weakly, correlated. Female coloration did not correlate with female ability to compensate for the loss of male care, or with the change in brood mass during male removal. Therefore, there is no evidence for the good-parent hypothesis to explain female plumage coloration in bluethroats. Received: 4 March 1999 / Received in revised form: 14 October 1999 / Accepted: 23 October 1999     

Female preference for symmetry in computer-animated three-spined sticklebacks,<Emphasis Type="Italic"> Gasterosteus aculeatus</Emphasis>

Fluctuating asymmetries are subtle random deviations from perfect symmetry in bilateral traits caused by the inability of individuals to buffer their development against the disruptive effects of genetic and environmental stresses. The degree of asymmetry of secondary sexual characters is supposed to convey information about a male's phenotypic and/or genetic quality, and females may thus be expected to use bilateral symmetry as a cue in mate choice. We independently and simultaneously manipulated the length and the relative symmetry of the pelvic spines of computer-animated three-spined sticklebacks, Gasterosteus aculeatus. In all mate choice tests involving two male models differing in spine symmetry, females preferred the symmetric model, irrespective of spine length, though only significantly so when both male models had short spines. Females did not significantly discriminate between male models differing in spine length alone. The preference for symmetry was stronger the higher the females' physical condition. Our study demonstrates that female sticklebacks master the perceptual abilities required to discriminate between potential mates basing exclusively on small length differences between paired structures, and provides experimental evidence that spine symmetry is subject to sexual selection through female choice in this species.     

Association patterns of sailfin mollies (Poecilia latipinna): alternative hypotheses

Individuals may associate with each other due to a variety of selective forces, such as intra- and intersexual selection, and conspecific recognition. Previous studies have concluded that mate choice governs association behavior in polygynous species of fish. I examined whether mate choice underlies the preference for larger individuals by examining preference for association (time spent in proximity to a fish) not only between opposite-sex individuals but also between same-sex individuals of the live-bearing sailfin molly (Poecilia latipinna). Males and females from three size classes were tested with a large and a small object fish of the same and opposite sex. Females preferred to associate with larger over smaller males. Males also preferred to associate with larger over smaller females, as expected. The same female and male test fish also preferred to associate with larger over smaller fish of the same sex. Moreover, females demonstrated no significant difference in their strength of preference (large–small) when offered males or females. The same held true for males. When males and females were subsequently tested with one large male and one large female, females tended to prefer large males while males showed no significant preference for association based on sex. In another experiment, females were tested with a large female and a small male, and significantly preferred the former. These findings suggest that association patterns may have arisen under a variety of conditions, such as predation pressures, shoaling behavior, and associative preference behavior. The assumption that association behavior is a uniformly sufficient predictor of mate choice in fish needs to be re-examined for P. latipinna and other species. Received: 6 November 1998 / Received in revised form: 12 May 1999 / Accepted: 12 May 1999     

Female resistance and male preference in a stream-dwelling isopod: effects of female molt characteristics

In the stream-dwelling isopod, Lirceus fontinalis, mating contests between males and females occur prior to pair formation. We examined the relative contribution of male preference and female resistance to contest outcomes. We first quantified male and female behavior during typical mating interactions and examined the relationship between time until molt (TTM) and mating outcomes. We then examined the role of male preference and female resistance in determining mating outcomes when females differed in molt type (growth, egg deposition) and appeared to differ in TTM (due to hormone applications). Both male preference and female resistance contributed to different components of the mating sequence but female resistance ultimately determined whether or not pair formation occurred. Males expressed a preference for females that appeared to be close to molt, using variation in levels of molt hormone as a cue. However, males did not discriminate between females based on molt type. Received: 5 March 1999 / Received in revised form: 10 August 1999 / Accepted: 16 October 1999     

Sequential female choice and the previous male effect in sticklebacks

Summary Female choice, identified as a major force in sexual selection theory, has recently been demonstrated in a number of species. These tests concentrated on simultaneous choice situations although females have to compare males sequentially in most territorial species, which is the more demanding task. Here it is shown that female three-spined sticklebacks, Gasterosteus aculeatus L., rate sequentially presented males according to their brightness. With increasing costs of sampling the females become less choosy. Furthermore, a male's attractiveness has a significant effect on the female's rating of the next male; a given male is rated higher when preceded by a duller male than by a brighter one and vice versa. Female sticklebacks use a stochastic decision rule in sequential mate choice that is attuned to the attractiveness of the present and previously encountered male. This demonstration of a previous male effect not only indicates an efficient mechanism for finding the best of a number of males but also extends the applicability of sexual selection theory.Offprint requests to: T.C.M. Bakker     

The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis nyererei complex)

We studied the effect of male coloration on interspecific female mate choice in two closely related species of haplochromine cichlids from Lake Victoria. The species differ primarily in male coloration. Males of one species are red, those of the other are blue. We recorded the behavioral responses of females to males of both species in paired male trials under white light and under monochromatic light, under which the interspecific differences in coloration were masked. Females of both species exhibited species-assortative mate choice when colour differences were visible, but chose non-assortatively when colour differences were masked by light conditions. Neither male behaviour nor overall female response frequencies differed between light treatments. That female preferences could be altered by manipulating the perceived colour pattern implies that the colour itself is used in interspecific mate choice, rather than other characters. Hence, male coloration in haplochromine cichlids does underlie sexual selection by direct mate choice, involving the capacity for individual assessment of potential mates by the female. Females of both species responded more frequently to blue males under monochromatic light. Blue males were larger and displayed more than red males. This implies a hierarchy of choice criteria. Females may use male display rates, size, or both when colour is unavailable. Where available, colour has gained dominance over other criteria. This may explain rapid speciation by sexual selection on male coloration, as proposed in a recent mathematical model. Received: 11 April 1997 / Accepted after revision: 27 July 1997     

Phenotypic differentiation in female preference related to geographic variation in male predation risk in the Trinidad guppy (Poecilia reticulata)

Summary Populations of the Trinidad guppy range from areas with high levels of predation by other species of fish to areas with little or no piscine predation. Previous studies have shown that variation among populations in male coloration can be explained by a balance between female preference for brighter males and natural selection against bright males. High levels of male courtship activity may also increase both predation risk and mating success. Therefore, in high-predation areas, females that mate with males that court frequently as well as those that choose bright males would presumably produce male offspring with low survivorship. Consistent with this variation in natural selection, we observed that females from high-predation populations were less likely to choose bright and frequently courting males than females from low-predation populations. This result supports the hypothesis that female preference is evolving as a character genetically correlated with the preferred male character, in which case higher levels of natural selection acting against the male character should be related to lower levels of female preference.     

Why insects swarm: testing the models for lek mating systems on swarming Empis borealis females

Summary Female dance-flies, Empis borealis L., gather to swarm, and males carrying nuptial gifts visit swarms for mating. Field observations and experiments were performed on this behaviorally sex-role reversed species to test models of lekking behavior. The key predictions were: (1) female preference model: male visiting rate and mating rate should increase with the number of females in swarm (swarm size), (2) hotspot model: male visiting rate should be independent of swarm size, and (3) hotshot model: swarm size should be positively correlated with the body size of the largest female in swarm. We found that male visiting rate and mating rate increased with swarm size, and that mating rate per female increased with swarm size. Males also mated more often in larger swarms than in smaller ones. Both males and females visited swarm sites even in the absence of other individuals. When females were successively removed from swarm sites more males than females on average arrived at these sites: 2.25 males per female. When no individuals were present at the swarm site, arriving males moved on to another site, whereas arriving females generally stayed. Larger experimental swarm-markers attracted both more males and more females and even more males when swarming females were present. There was no correlation between mean or median female size in swarms and the number of females in swarms. Thus, the female preference model and the hotspot model were corroborated, while other models were judged unlikely to explain swarming behavior in E. borealis. Correspondence to: B.G. Svensson     

Female choice on male quantitative traits in lizards — why is it so rare?

Female choice on the basis of male traits has been described in an array of taxa but has rarely been demonstrated in reptiles. In the sand lizard (Lacerta agilis), and possibly in other non-territorial reptiles, a male's contribution to a female's fitness is restricted to his genes. In order to choose males of high genetic quality, females have to trade the fitness gain against the costs of active choice. In a Swedish population of sand lizards, long-lived males sired offspring with higher embryonic survival compared to offspring sired by short-lived males. In spite of this female sand lizards did not mate selectively with older and/or larger males. There appeared to be mo reliable cues to male longevity; age-specific male body size was highly variable. Furthermore, estimates of male nuptial coloration did not covary with ectoparasite load and, hence, females cannot use male coloration as a cue to heritable resistance to pathogenic parasite effects. When cues to male genetic quality are poor, or inaccurate, and males make no parental investment, we predict that female choice will be rare. Sand lizard females mating with many partners lay clutches with higher hatching success. Thus, females may obtain good genes for their young by multiple mating, thereby avoiding costs associated with mate choice.     

Responses of female lizards,<Emphasis Type="Italic"> Lacerta monticola</Emphasis>, to males' chemical cues reflect their mating preference for older males

Female mate choice based on visual traits appears to be rare in lizards. Field observations suggest that females of the lizard Lacerta monticola preferred to mate with larger/older males. Although older males are usually green and larger, and younger males brown and smaller, there is some overlap in size and coloration between age classes. Thus, visual cues may not always be reliable indicators of a male's age. We hypothesized that female mate-choice preferences may be based on males' pheromones, which might transmit information about characteristics such as age. In a laboratory experiment, we analyzed the effect of age of males on attractiveness of their scents to females. When we offered scents of two males of different age, females associated preferentially with scents of older males. This suggested that females were able to assess the age of males by chemical signals alone, and that females preferred to be in areas scent-marked by older males. Thus, females may increase their opportunities to mate with males of high quality, or may avoid harassment by sneaking young males. This result agreed with field observations on females mating with old males, and rejection of advances by young males. Our results also suggested that female preference for older males may depend on their own body size. Large females showed a strong preference for older males, whereas smaller females were not so selective. This, together with males' preference for large females, might lead to size-assortative matings. We suggest that the quality and/or quantity of male pheromones could communicate to the female heritable male genetic quality (i.e. age) and thereby serve as the basis of adaptive female choice in lizards.Communicated by W.E. Cooper