Sexually selected male weapon is associated with lower inbreeding load but higher sex load in the bulb mite

Elaborate sexually selected ornaments and armaments are costly but increase the reproductive success of their bearers (usually males). It has been postulated that high-quality males can invest disproportionately more in such traits, making those traits honest signals of genetic quality. However, genes associated with such traits may have sexually antagonistic effects on fitness. Here, using a bulb mite Rhizoglyphus robini, a species in which a distinct dimorphism exists between males in the expression of a sexually selected weapon, we compare inbreeding and gender load between lines derived from armed fighters and unarmed scramblers. After four generations of sib-mating, inbreeding depression for female fitness was significantly lower in fighter-derived lines compared to scrambler-derived lines, suggesting that fighter males had significantly higher genetic quality. However, outbred females from fighter-derived lines had significantly lower fitness compared to outbred females from scrambler-derived lines, demonstrating significant gender load associated with the presence of a sexually selected male weapon. Our results imply that under outbreeding, genetic benefits of mating with bearers of elaborate sexually selected traits might be swamped by the costs of decreased fitness of female progeny due to sexually antagonistic effects.     

Socially selected ornaments and fitness: Signals of fighting ability in paper wasps are positively associated with survival,reproductive success,and rank

Many animals have ornaments that mediate choice and competition in social and sexual contexts. Individuals with elaborate sexual ornaments typically have higher fitness than those with less elaborate ornaments, but less is known about whether socially selected ornaments are associated with fitness. Here, we test the relationship between fitness and facial patterns that are a socially selected signal of fighting ability in Polistes dominula wasps. We found wasps that signal higher fighting ability have larger nests, are more likely to survive harsh winters, and obtain higher dominance rank than wasps that signal lower fighting ability. In comparison, body weight was not associated with fitness. Larger wasps were dominant over smaller wasps, but showed no difference in nest size or survival. Overall, the positive relationship between wasp facial patterns and fitness indicates that receivers can obtain diverse information about a signaler's phenotypic quality by paying attention to socially selected ornaments. Therefore, there are surprisingly strong parallels between the information conveyed by socially and sexually selected signals. Similar fitness relationships in social and sexually selected signals may be one reason it can be difficult to distinguish the role of social versus sexual selection in ornament evolution.     

The evolution of sexually selected traits and antagonistic androgen expression in actinopterygiian fishes

Many sexually selected traits in male fishes are controlled by testosterone. Directional selection for male ornaments could theoretically increase male testosterone levels over evolutionary timescales, and when genetically correlated, female testosterone levels as well. Because of the negative fitness consequences of high testosterone, it is plausible that female choice for sexually selected traits in males results in decreased female reproductive fitness. I used comparative analysis to examine the association between male peak testosterone expression and sexually selected ornaments. I also tested for genetic correlation between male and female androgen levels. The presence of sexually selected traits in males was significantly correlated with increased peak androgen levels in males as well as females, and female testosterone levels were significantly correlated with male peak testosterone titers, although the slope was only marginally <1. This suggests that selection to decouple high male and female testosterone levels is either weak or otherwise ineffective.     

Ornaments or offspring: costs to reproductive success restrict sexual selection processes

If, in their partner choice, males seek direct benefits (fecund females), the result will be selection for traits indicating female quality rather than for arbitrary (Fisherian) traits. However, the costs of developing and maintaining the sexually selected traits (ornaments) may reduce the resources available to the female for allocation to reproduction and hence result in lower reproductive success per brood. This hitherto unrecognized fecundity cost of sexually selected traits will constrain both the potency of sexual selection mechanisms and the degree of elaboration of sexually selected traits in females, and can also apply to males which invest in their offspring: sexual selection becomes self-limiting. The fitness implications of these costs are examined for both sexes in a variety of mating and parental care patterns. Sexual selection acting on both sexes may lead to either dimorphism or monomorphism, the latter being the case when the quality indicators chosen by both sexes coincide. Ways of evasion or reduction of these reproductive costs of allocations to sexually selected traits include using different resource components for the ornament and for reproduction, or partitioning the two allocations in time.     

Geographic variation in the function of ornaments in the common yellowthroat Geothlypis trichas

We used controlled aviary experiments to study the role of male ornaments in male-male competition and female choice in the common yellowthroat Geothlypis trichas , a sexually dichromatic warbler. Previous aviary studies in Wisconsin, USA, indicated that males with larger black facial masks were dominant over males with smaller masks and preferred by females in mate choice experiments. In this study, we replicated those experiments in a population in New York, USA, where male mating success was related more consistently to the size of the yellow bib (throat, breast, and belly) than to the size of the mask. Similar to the study in Wisconsin, we found that males with larger masks were more likely to be dominant in New York, however, we found that males with larger bibs were preferred by females in New York, and there was no significant preference for males with larger masks. These results are consistent with the hypothesis that carotenoid-based ornaments are selected by female choice and melanin-based ornaments are selected by male-male competition. However, the pattern of female choice appears to vary between New York and Wisconsin. This geographic difference could be related to a variety of environmental factors (habitat, carotenoid and parasite abundance) that affect the costs and benefits of choosing males with particular ornaments in each location.     

Conditional expression of a sexually selected trait in the stalk-eyed fly Diasemopsis aethiopica

1. An important assumption of many models of the evolution of sexually selected ornaments is that such ornaments should be conditionally expressed. This was investigated by rearing larvae of the stalk-eyed fly Diasemopsis aethiopica (Diptera: Diopsidae) (Rondani) on two food treatments: normal and low-quality food. 2. Female flies responded to better food by increasing both their body size and the relative length of their eyestalks. 3. Male flies responded by increasing only the length of their eyestalks. 4. This demonstrates that food quality can change the allometric relationship between body size and the size of a sexually selected character in this species, and gives an insight into the different developmental priorities of each sex in this species.     

Environmentally realistic exposure to the herbicide atrazine alters some sexually selected traits in male guppies

Male mating signals, including ornaments and courtship displays, and other sexually selected traits, like male-male aggression, are largely controlled by sex hormones. Environmental pollutants, notably endocrine disrupting compounds, can interfere with the proper functioning of hormones, thereby impacting the expression of hormonally regulated traits. Atrazine, one of the most widely used herbicides, can alter sex hormone levels in exposed animals. I tested the effects of environmentally relevant atrazine exposures on mating signals and behaviors in male guppies, a sexually dimorphic freshwater fish. Prolonged atrazine exposure reduced the expression of two honest signals: the area of orange spots (ornaments) and the number of courtship displays performed. Atrazine exposure also reduced aggression towards competing males in the context of mate competition. In the wild, exposure levels vary among individuals because of differential distribution of the pollutants across habitats; hence, differently impacted males often compete for the same mates. Disrupted mating signals can reduce reproductive success as females avoid mating with perceptibly suboptimal males. Less aggressive males are at a competitive disadvantage and lose access to females. This study highlights the effects of atrazine on ecologically relevant mating signals and behaviors in exposed wildlife. Altered reproductive traits have important implications for population dynamics, evolutionary patterns, and conservation of wildlife species.     

Multiple ornaments are positively related to male survival in the common pheasant

Several empirical studies have reported a positive relation between male viability and the expression of sexually selected traits, but others have reported a significant negative relation. Using the ability to evade predators as an indicator of male viability, we evaluated the direction of this relationship in a free-ranging population of common pheasants,Phasianus colchicus , which have multiple ornaments and are sexually dimorphic in tail length and in ornaments such as wattles and tarsal spurs. We translocated 72 males into a protected area and radiotracked them during the breeding seasons of 3 years. Before releasing them, we measured their body weight, wing and tail length, wattle height and spur length. Male survivors had larger multiple ornaments, regardless of age, than males that were killed by predators but survival selection on wing length and body weight was nonsignificant, showing that selection on male ornaments was not the result of selection on correlated traits.Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

The Evolution of Wing Shape in Ornamented-Winged Damselflies (Calopterygidae, Odonata)

Flight has conferred an extraordinary advantage to some groups of animals. Wing shape is directly related to flight performance and evolves in response to multiple selective pressures. In some species, wings have ornaments such as pigmented patches that are sexually selected. Since organisms with pigmented wings need to display the ornament while flying in an optimal way, we might expect a correlative evolution between the wing ornament and wing shape. We examined males from 36 taxa of calopterygid damselflies that differ in wing pigmentation, which is used in sexual displays. We used geometric morphometrics and phylogenetic comparative approaches to analyse whether wing shape and wing pigmentation show correlated evolution. We found that wing pigmentation is associated with certain wing shapes that probably increase the quality of the signal: wings being broader where the pigmentation is located. Our results also showed correlated evolution between wing pigmentation and wing shape in hind wings, but not in front wings, probably because hind wings are more involved in signalling than front wings. The results imply that the evolution of diversity in wing pigmentations and behavioural sexual displays might be an important driver of speciation due to important pre-copulatory selective pressures.     

Elevating perceived predation risk modifies the relationship between parental effort and song complexity in the song sparrow Melospiza melodia

Adult‐directed predation risk elevates costs of parental care, and may modify relationships between sexually selected ornaments and parental effort by accentuating the tradeoff between survival and parental investment. We assessed multiple hypotheses regarding the relationship between maternal effort, paternal effort, and the sexually selected trait of male song complexity in the song sparrow Melospiza melodia. Further, we explored whether experimentally elevating perceived adult‐directed predation risk near nests affected these relationships. We quantified two dimensions of song complexity: song repertoire size and residual syllable number (the relative number of syllables for a given song repertoire size). Under elevated perceived predation risk, but not in the absence of the predator stimuli, females mated to males with higher residual syllable number displayed higher nestling provisioning rates and performed a greater proportion of nestling provisioning trips. In other words, elevating perceived predation risk induced a pattern of maternal investment consistent with differential allocation. In contrast, under elevated perceived predation risk, only, females performed a lesser proportion of provisioning trips when mated to males with large song repertoire sizes. Further, consistent with the good parent hypothesis, males with large song repertoire sizes displayed lower latencies to return to the nest, independent of the predator stimuli. Results suggest that residual syllable number may reflect some aspect of male genetic quality, such that females are more willing to maintain maternal effort while facing heightened predation risk. On the other hand, females may gain paternal benefits when mated to males with large song repertoires. Our study supports the hypothesis that increased costs of parental care associated with predation risk may induce relationships between sexually selected traits and parental behavior, which may increase the strength of sexual selection. Additionally, results suggest that different aspects of song complexity may fulfill non‐equivalent signaling roles.     

Patterns of variation in tail ornament size in birds

In recent years several different kinds of sexual selection models have been developed, and tail ornaments in birds have frequently been used as an example of a sexually selected character where the models might apply. However, very little is known about intra- and interpopulation variation in ornament size. We have studied the elongated tail ornaments in four species of whydahs Vidua , the forktailed flycatcher Tyrannus savana and the Asian paradise flycatcher Terpsiphone paradisi. Ornaments were relatively longer in males with the longest tarsi ('heterogony' with positive allometry). Also, tail lengths were remarkably variable within each geographical area, the coefficient of variation (average = 11%) being three times as high as for body size characters. Models, with female preference of ornaments bearing no relation to male viability, usually generate lines of neutral equilibria. Thus, they predict extraordinary variation in ornaments between populations. However, elongated tail ornaments did not show higher geographical variation than the body size characters, suggesting that there is no line of equilibria for these ornaments.     

A trade-off between reproduction and a condition-dependent sexually selected ornament in the house sparrow Passer domesticus

Reproductive effort was manipulated in a free-living population of house sparrows (Passer domesticus) to investigate the trade-off between reproductive investment and the expression of a condition-dependent sexually selected ornament. Phenotypic plasticity in the expression of this trait was related to the experimentally manipulated size of the brood reared by a male. Males that invested more in current reproduction subsequently became more attractive to females in this population as they showed a preference for males with smaller badges. This supports the argument that direct benefits are a primary focus for mate choice by females. Trade-offs between reproductive effort and the expression of sexual ornaments are a potentially important source of phenotypic variation in both sexual ornaments and life-history traits.     

Testing the functional significance of tail streamers

Studies of the evolution of elaborate ornaments have concentrated on their role in increasing attractiveness to mates. The classic examples of such sexually selected structures are the elongated tails of some bird species. Elongated tails can be divided into three categories: graduated tails, pin tails and streamers. There seems to be little debate about whether graduated and pin tails are ornaments; i.e. costly signals used in mate choice. However, in the case of streamers there is considerable discussion about their function. It has been suggested that tail streamers could be (i) entirely naturally selected, (ii) entirely sexually selected, (iii) partly naturally and partly sexually selected. The prime example of a species with tail streamers is the swallow (Hirundo rustica) in which both sexes have tail streamers. In this paper we discuss the aerodynamic consequences of different types of manipulation of the streamer and/or outer tail feather. We make qualitative predictions about the aerodynamic performance of swallows with manipulated tail streamers; these predictions differ depending on whether streamers have a naturally or sexually selected function. We demonstrate that these hypotheses can only be separated if tail streamers are shortened and changes in aerodynamic performance measured during turning flight.     

Sexually selected sexual selection: Can evolutionary retribution explain female ornamental colour?

By preferring mates with increasingly costly ornaments or courtship displays, females cause an escalation of male reproductive costs. Such increased costs should promote male selectivity based on fecundity‐linked female attributes, leading to female ornamentation in species with traditional sex roles. Consequently, female ornamentation should evolve more frequently in taxa where male reproduction is costly than in comparable taxa where it is cheaper. We assessed the prevalence of female ornamental colouration in two clades of viviparous cyprinodontid fish: the Goodeinae, where stringent female choice imposes male mating costs, and the Poeciliinae, whose males can circumvent female mate choice. We found that although in the Poeciliinae female ornamental colour is a correlated, but paler version of male coloration, females of the Goodeinae often display vivid ornamental colours that are distinct from those of males. Thus, male and female ornaments are not (phylo)genetically correlated in the Goodeinae. Furthermore, phylogenetic signal on male and female colour is clearly detectable in the Poeciliinae, but absent in the Goodeinae, suggesting that ornamental colour of males and females in the latter may be the consequence of selection. Given that enforceable female choice has promoted male ornaments, we propose that evolutionary retribution has promoted distinct female ornaments in the Goodeinae.     

The immunocompetence handicap hypothesis: testing the genetic predictions

The immunocompetence handicap hypothesis suggests that the immune system competes for resources with sexually selected ornaments; variation in ornaments might reflect genetic variation for immunocompetence. We tested this genetic prediction by mating scorpionfly females to males differing in the expression of a condition-dependent ornament trait, saliva secretion, and then comparing offspring immunocompetence. We found several indications of an immunocompetence handicap in our study: females had superior immunocompetence compared with males, the different immune traits were positively correlated, and there were indications of genetic variation in immune traits. However, we found no significant difference in the immunocompetence of offspring derived from males differing in ornament expression, only a tendency for sons of ornamented males to possess slightly better immunocompetence. The estimated effect of fathers on offspring immunocompetence was rather small, but it might be a sufficient benefit of female choice, provided that the costs of choice are small. We conclude that the genetic benefit of female choice is small concerning offspring immunocompetence, but the immunocompetence handicap principle might nevertheless work in scorpionflies.     

The sexual selection paradigm: have we overlooked other mechanisms in the evolution of male ornaments?

Extravagant male ornaments expressed during reproduction are almost invariably assumed to be sexually selected and evolve through competition for mating opportunities. Yet in species where male reproductive success depends on the defence of offspring, male ornaments could also evolve through social competition for offspring survival. However, in contrast to female ornaments, this possibility has received little attention in males. We show that a male ornament that is traditionally assumed to be sexually selected—the red nuptial coloration of the three-spined stickleback—is under stronger selection for offspring survival than for mating success. Males express most coloration during parenting, when they no longer attract females, and the colour correlates with nest retention and hatching success but not with attractiveness to females. This contradicts earlier assumptions and suggests that social selection for offspring survival rather than for sexual selection for mating success is the main mechanism maintaining the ornament in the population. These results suggest that we should consider other forms of social selection beyond sexual selection when seeking to explain the function and evolution of male ornaments. An incorrect assignment of selection pressures could hamper our understanding of evolution.     

Sexually selected traits and adult survival: a meta-analysis

Traits correlated with male mating success are likely to be subject to sexual selection. Sexually selected characters are thought to be costly to develop and maintain. If males do not vary their investment in sexual traits in relation to their ability to bear the costs, there should be a negative relationship between male longevity or survival and the expression of sexual traits. In particular, a negative relationship is predicted by pure Fisherian models for the evolution of sexual ornaments. The same should also be true for traits that evolve via pleiotropy (e.g., due to sensory exploitation or bias) with no subsequent evolution of condition dependent modification. We collected information on the relationship between traits correlated with male mating rate and estimates of adult male survivorship or life span. In total we obtained 122 samples from 69 studies of 40 species of bird, spider, insect, and fish. In a meta-analysis we calculated the average sample size weighted correlation between trait expression and adult survival. Analyses at the level of samples, studies, and species revealed significant positive relationships (r = 0.08, 0.10, and 0.13, respectively; all P < 0.001). The unweighted correlation at the species level was r = 0.24. In general, males with larger ornaments or weapons, greater body size, or higher rates of courtship showed greater survivorship or longevity. This finding is inconsistent with pure Fisherian models or other models that do not incorporate condition or quality dependent trait expression. It suggests that male investment in sexually selected traits is not fixed but varies in relation to the ability to pay the underlying costs of expressing these characters. Hence, many secondary sexual characters are likely to be condition dependent in their expression.     

Condition‐dependence and sexual ornamentation: Effects of immune challenges on a highly sexually dimorphic grasshopper

Sexual ornaments contribute substantially to phenotypic diversity and it is particularly relevant to understand their evolution. Ornaments can assume the function of signals‐of‐quality that the choosy sex uses to evaluate potential mating partners. Often there are no obvious direct benefits and investment into mate choice is primarily rewarded by beneficial alleles that are inherited to the offspring. Inter‐sexual communication via sexual ornaments requires honesty of the sexual signal, yet the question of what maintains honesty remains only partially solved. One solution is that honesty is maintained by trait expression being dependent on individual condition, since condition‐dependent trait expression offers an effectively inexhaustible source of genetic variability. Here we test in the highly sexually dimorphic club‐legged grasshopper Gomphocerus sibiricus if putative sexual ornaments, in particular the striking front‐leg clubs, are more strongly affected by a lipopolysaccharide (LPS) immune challenge than putatively not sexually selected traits. Our results show overall little condition‐dependent expression of morphological and song traits, with sexually selected traits exhibiting effects comparable to nonsexually selected traits (with the possible exception of stridulatory file length and syllable‐to‐pause ratio in advertisement songs). Interestingly, field observations of individuals of lethally parasitized individuals suggest that a very strong environmental challenge can specifically affect the expression of the front‐leg clubs. The presence of 1% of males in natural populations with missing or heavily deformed clubs plus 5% with minor club deformations furthermore indicate that there are risks associated with club development during final ecdysis and this might act as a filter against deleterious alleles.     

Sex chromosomes and male ornaments: a comparative evaluation in ray-finned fishes

Theory predicts that the mechanism of genetic sex determination can substantially influence the evolution of sexually selected traits. For example, female heterogamety (ZZ/ZW) can favour the evolution of extreme male traits under Fisher's runaway model of sexual selection. We empirically test whether the genetic system of sex determination has played a role in the evolution of exaggerated male ornaments in actinopterygiian fishes, a clade in which both female-heterogametic and male-heterogametic systems of sex determination have evolved multiple times. Using comparative methods both uncorrected and corrected for phylogenetic non-independence, we detected no significant correlation between sex-chromosome systems and sexually selected traits in males. Results suggest that sex-determination mechanism is at best a relatively minor factor affecting the outcomes of sexual selection in ray-finned fishes.     

Maintenance of variation in sexually selected traits in females: a case study using intrasexual aggression in tree swallows Tachycineta bicolor

A fundamental question in evolutionary biology is how phenotypic variation is maintained in the face of selection that ought to deplete that variation. Much research has investigated this question in traits favored via sexual selection in males, with a common solution implicating the condition dependence of sexually selected phenotypes. Despite growing interest in sexual selection on females, it is not clear if the same mechanisms maintain variation in female ornaments, weaponry or other female behaviors targeted by sexual selection. An important step in testing condition dependence in females is thus to identify whether sexually selected female phenotypes are associated with condition and also with potential costs. Here, I examine these two components of condition dependence for a sexually selected behavior, intrasexual aggression, in female tree swallows Tachycineta bicolor. I asked whether high levels of intrasexual aggression map onto natural variation in female condition and whether aggression is associated with one potential behavioral cost: performance in a vertically challenging test of flight. More aggressive females were heavier for their body size, heavier for their wing size and showed decreased flight ability, relative to less aggressive females. These findings are consistent with condition dependence, where only females in better condition are able to be highly aggressive. The association between high aggression and reduced flight ability may result from the additional lift required to power these relatively heavier birds. These associations between natural variation in aggressive behavior, morphology and flight ability are consistent with condition dependence because they confirm two basic assumptions of condition dependence: a link between aggression and condition, and a link between aggression and a behavioral cost, the speed of escape flight. As the first study to examine these assumptions for a conspicuous behavior favored by intrasexual selection in females, this study suggests broad relevance of condition dependence.