Phenotypic variance in an acoustic signal: a potentially sexually selected behaviour in Cape Clapper Larks Corypha apiata

Is sexual selection beneficial during adaptation to environmental change?

Models of sexual selection predict that females use ornament size to evaluate male condition. It has also been suggested that ornament asymmetry provides females with accurate information about condition. To test these ideas we experimentally manipulated condition in the stalk-eyed fly, Cyrtodiopsis dalmanni, by varying the amount of food available to developing larvae. Males of this species have greatly exaggerated eyestalk length and females prefer to mate with males with wider eyespans. Our experiments show that male ornaments (eyestalks) display a disproportionate sensitivity to condition compared with the homologous character in females, and to non-sexual traits (wing dimensions). In contrast, in neither sex did asymmetry reflect condition either in sexual ornaments or in non-sexual traits. We conclude that ornament size is likely to play a far greater role in sexual selection as an indicator of individual condition than does asymmetry.

A "Good-Sperm" Model Can Explain the Evolution of Costly Multiple Mating by Females

Interactions between natural and sexual selection have been integral to the development of sexual selection theory, yet the role of natural selection in sexual trait evolution has received far less empirical attention than the role of sexual selection, and the extent to which natural and sexual selection are aligned remains an important empirical question. Insect cuticular hydrocarbons (CHCs) provide a good model for exploring interactions between natural and sexual selection because of their dual roles in sexual signalling and desiccation resistance. We used the geometric framework for nutrition to explore the potential for, and magnitude of trade‐offs between male attractiveness, desiccation resistance and the abundance and blend of CHCs in the cricket Teleogryllus oceanicus . Attractiveness and desiccation resistance were both maximized on a diet that was rich in carbohydrate relative to protein. Although maximum expressions occurred at significantly different locations in nutritional space, the difference in angles between maximum attractiveness and desiccation resistance were small. Attractiveness and desiccation resistance were both associated with CHCs of moderate, rather than maximum, abundance and with a blend that was rich in two shorter chained alkenes relative to a single longer chained alkane. Partial correlations between fitness traits suggested that CHCs contribute indirectly to male attractiveness via their role in desiccation resistance. Our findings are consistent with the idea that natural and sexual selection on CHCs can be broadly aligned, facilitating rapid adaptation to ecological conditions and promoting speciation. Read the free Plain Language Summary for this article on the Journal blog.

The evolution of sexual display traits or preferences for them in response to divergent natural selection will alter sexual selection within populations, yet the role of sexual selection in ecological speciation has received little empirical attention. We evolved 12 populations of Drosophila serrata in a two-way factorial design to investigate the roles of natural and sexual selection in the evolution of female mate preferences for male cuticular hydrocarbons (CHCs). Mate preferences weakened in populations evolving under natural selection alone, implying a cost in the absence of their expression. Comparison of the vectors of linear sexual selection revealed that the populations diverged in the combination of male CHCs that females found most attractive, although this was not significant using a mixed modelling approach. Changes in preference direction tended to evolve when natural and sexual selection were unconstrained, suggesting that both processes may be the key to initial stages of ecological speciation. Determining the generality of this result will require data from various species across a range of novel environments.

Sexual Selection and Variance in Reproductive Success

Rapid diversification is common among herbivorous insects and is often the result of host shifts, leading to the exploitation of novel food sources. This, in turn, is associated with adaptive evolution of female oviposition behavior and larval feeding biology. Although natural selection is the typical driver of such adaptation, the role of sexual selection is less clear. In theory, sexual selection can either accelerate or impede adaptation. To assess the independent effects of natural and sexual selection on the rate of adaptation, we performed a laboratory natural selection experiment in a herbivorous bruchid beetle (Callosobruchus maculatus). We established replicated selection lines where we varied natural (food type) and sexual (mating system) selection in a 2 x 2 orthogonal design, and propagated our lines for 35 generations. In half of the lines, we induced a host shift whereas the other half was kept on the ancestral host. We experimentally enforced monogamy in half of the lines, whereas the other half remained polygamous. The beetles rapidly adapted to the novel host, which primarily involved increased host acceptance by females and an accelerated rate of larval development. We also found that our mating system treatment affected the rate of adaptation, but that this effect was contingent upon food type. As beetles adapted to the novel host, sexual selection reinforced natural selection whereas populations residing close to their adaptive peak (i.e., those using their ancestral host) exhibited higher fitness in the absence of sexual selection. We discuss our findings in light of current sexual selection theory and suggest that the net evolutionary effect of reproductive competition may critically depend on natural selection. Sexual selection may commonly accelerate adaptation under directional natural selection whereas sexual selection, and the associated load brought by sexual conflict, may tend to depress population fitness under stabilizing natural selection.

There is a growing effort to understand how sexual selection varies over space and time under different ecological conditions and how this can maintain variation in sexual traits. An interesting ecological condition is population density, which can either increase or decrease sexual selection depending on the natural history of the species. We examined sexual and natural selection in an undescribed amphipod species (Hyalella sp.) using surveys of two natural populations that increase in density from spring to summer. We also conducted an experiment that directly manipulated density to assess the effects on sexual selection. In the field during spring (low density) and summer (high density), we documented sexual selection on male traits, including body size, gnathopods and antennae. We found that the magnitude and direction of this selection changed from spring to summer and that selection patterns differed between populations. In the experiment, we found no sexual selection occurred at low density, but found significant positive selection on all three male traits at medium and high densities. These results underline the importance of isolating individual ecological factors to determine their role in sexual selection while also documenting patterns in natural populations to understand how selection varies over space and time.

Male–male competition and female mate choice act contemporaneously in the cockroach Nauphoeta cinerea and the social pheromone of males influences the outcome of both forms of sexual selection. We therefore examined the joint and separate effects of male–male competition and female mate choice to determine if the selective optima for the pheromone were the same or different. Dominant males in a newly established hierarchy mated more frequently, but not exclusively. Manipulations of the multi-component social pheromone produced by males of N. cinerea showed that both long- and close-range attraction of females by males were influenced by the quantity and composition of the pheromone. The most attractive composition, however, differed from that which was most likely to confer high status to males. Since the outcome of male–male competition can conflict with mating preferences exhibited by females, there is balancing sexual selection on the social pheromone of N. cinerea. Such balancing selection might act to maintain genetic variation in sexually selected traits. We suggest that the different forms of sexual selection conflict in N. cinerea because females prefer a blend different to that which is most effective in male–male competition in order to avoid mating with overly aggressive males.

The role of sexual selection in speciation is investigated, addressing two main issues. First, how do sexually selected traits become species recognition traits? Theory and empirical evidence suggest that female preferences often do not evolve as a correlated response to evolution of male traits. This implies that, contrary to runaway (Fisherian) models of sexual selection, premating isolation will not arise as an automatic side effect of divergence between populations in sexually selected traits. I evaluate premating isolating mechanisms in one group, the birds. In this group premating isolation is often a consequence of sexual imprinting, whereby young birds learn features of their parents and use these features in mate choice. Song, morphology and plumage are known recognition cues. I conclude that perhaps the main role for sexual selection in speciation is in generating differences between populations in traits. Sexual imprinting then leads to these traits being used as species recognition mechanisms. The second issue addressed in this paper is the role of sexual selection in adaptive radiation, again concentrating on birds. Ecological differences between species include large differences in size, which may in themselves be sufficient for species recognition, and differences in habitat, which seem to evolve frequently and at all stages of an adaptive radiation. Differences in habitat often cause song and plumage patterns to evolve as a result of sexual selection for efficient communication. Therefore sexual selection is likely to have an important role in generating premating isolating mechanisms throughout an adaptive radiation. It is also possible that sexual selection, by creating more allopatric species, creates more opportunity for ecological divergence to occur. The limited available evidence does not support this idea. A role for sexual selection in accelerating ecological diversification has yet to be demonstrated.

Sensory systems are important for any life task of an animal. Vision, and colour vision in particular, is essential for visual–based insects, such as Odonata (damselflies and dragonflies), many of which display colour patterns on their bodies. Numerous behavioural studies suggest that the diverse colour patterns function as a means for intersexual, intrasexual, interspecific, or intraspecific recognition and play a role in sexual selection, particularly in ischnuran damselflies that have sex-limited polymorphism. However, to date there are no comprehensive studies linking behavioural to electrophysiological evidence to support the role of colour patterns and colour vision in mate choice in this group of insects. In my Ph.D. thesis, I investigated the function of body colouration and colour vision in sexual selection and communication of the Australian polymorphic damselfly, Ischnura heterosticta, and examined the mechanisms underlying its colour vision and colour discrimination ability. In an observational study (Chapter 2), I surveyed I. heterosticta reproductive behaviours and daily activity patterns in the field, providing the first detailed account of their colour morphs and behavioural biology. Andromorph females are blue like males, and gynomorph females have colour morphs in green, intermediate, and grey. Mating pairs, usually with gynomorphs, are formed after dawn and mating can last up to 3-4 hours. Oviposition occurs in the days after mating, and ovipositing females are subjected to aggressive male harassment, which varies with female colouration. These data provided the biological foundation regarding colour-based sexual selection in I. heterosticta investigated in the following chapters. In the next set of experiments (Chapter 3), I discovered a unique irreversible ontogenetic colour change in females of I. heterosticta: blue andromorphs are sexually immature individuals that emerge from nymphs. After 4 to 7 days, they turn into green-grey gynomorphs to signal their sexual maturity and advertise readiness to mate. Gynomorphs are the preferred mating partners, which suggests that blue andromorphs avoid unnecessary long mating during sexual immaturity through their male-mimicking colouration. This discovery provided the first indication that colour plays a key role in mate choice and that female polymorphism in I. heterosticta may be maintained via colour signals. In the next study (Chapter 4), I tested whether and how male mating preference was associated with colour cues by manipulating female body colours artificially. The outcomes strongly suggest that female body colouration is the key visual signal for mate choice in I. heterosticta. Males always preferred gynomorph females irrespective of female ratio or prior mating experience. Only under low ambient light males of I. heterosticta occasionally misidentified blue andromorphs as mating partners, likely as consequence of the insufficient light. This finding provided the behavioural indication that ischnuran damselflies rely on colour vision for mate recognition. The next study (Chapter 5) examined the morphological structure of the compound eyes of I. heterosticta using histological approaches. The diameter of an ommatidium is about 10 μm, and its length can be up to 400 μm depending on the area of the retina. Several retinula cells were identified distributed along the ommatidium. This provided essential background information on the visual anatomy in this species, and the anatomical indication that I. heterosticta may have colour vision, which was investigated in the next chapter. I used electrophysiological approaches (Chapter 6) to investigate the spectral sensitivities of the visual system of I. heterosticta. The results showed that they have trichromatic vision, being able to detect UV, blue and green light. Contrast calculations confirmed that their colour discrimination ability enables them to distinguish the spectral differences of individual female morphs. These results were congruent with the behavioural findings from previous chapters, showing that I. heterosticta use colour signals for mate choice in context of sexual selection. The final study (Chapter 7) examined the molecular basis of colour vision in I. heterosticta, and investigated whether it is plastic and dependent on light experience. I identified three types of opsin genes in I. heterosticta, corresponding to three wavelengths of light (UV, blue and green), confirming that this species is trichromatic. I found that during development opsins are differentially expressed in nymphs (aquatic) and adults (terrestrial/aerial), and opsin expression also changes when individuals are reared or kept under different ambient light conditions. These findings were further supported by electrophysiological experiments, showing an equivalent change in response. This demonstrates that colour vision in I. heterosticta is plastic and that ambient light induces visual plasticity. This plasticity facilitates adaptation to the changing visual environments during development, and ensures that adults can detect the crucial colour cues that are key for mate choice and reproduction. This thesis is the first comprehensive study examining the functional role of colour vision and body colouration in a polymorphic ischnuran damselfly. This body of work also contributes important new insights into the mechanisms underlying sexual selection, evolution and maintenance of female-limited polymorphism in I. heterosticta.

Developmental stability reflects the ability of individuals to cope with their environment during ontogeny given their genetic background. An inability to cope with environmental and genetic perturbations is reflected in elevated levels of fluctuating asymmetry and other measures of developmental instability. Both trait size and symmetry have been implicated as playing an important role in sexual selection, although their relative importance has never been assessed. We collected information on the relationship between success in sexual competition and size and asymmetry, respectively, to assess the relative importance of these two factors in sexual selection. Studies that allowed comparison of the relationships for the same traits' size and symmetry and success in sexual competition constituted the data, which totaled 73 samples from 33 studies of 29 species. The average sample-size weighted correlation coefficients between mating success or attractiveness and size and asymmetry, respectively, were used as measures of effect size in a meta-anatysis. Analysis was conducted on samples, studies, and species separately. We found evidence of an overall larger effect of symmetry at the species level of analysis, but similar effects at the sample or study levels. The difference in effect size for character size and character symmetry was larger for secondary sexual characters than for ordinary morphological characters at the level of analysis of samples. The results lend support to the conclusion that symmetry plays an important general role in sexual selection, especially symmetry of secondary sexual characters.

Reproduction is costly and individual decisions about when and how much to invest in reproduction will relate to potential benefits in terms of offspring survivorship or mating success. For those organisms that can reproduce more than once, individuals should invest relatively more in reproduction when the potential benefits are high. If females gain directly or indirectly from choosing attractive, highly ornamented males, then it could be predicted that females mated to these males should invest more in reproduction. Here we report the first test of this prediction for a lekking species, peafowl (Pavo cristatus), in which males do not provide resources for offspring, and females prefer to mate with those males that possess the most elaborate trains. We find that peahens randomly mated to males that vary in the degree of ornament produce more eggs for those peacocks with more elaborate trains. We could find no evidence to support the possibility that this difference arises as a result of difference between males in their ability to fertilize eggs.

The role of sexual selection in mediating levels of sexual conflict has been demonstrated in many experimental evolution studies on Drosophila spp. where competition among males for mating was the target of selection. Sexual selection has also been shown to affect the evolution of life-histories. However, the influence of divergent life-histories on reproductive strategies and, therefore, sexual selection and possibly sexual conflict has been less well studied. We examined D. melanogaster populations selected for a short development time and early age at reproduction for changes in reproductive behavior and traits that are proxies of sexual selection. We report a large reduction in reproductive competition experienced by the males of these populations, compared to ancestral populations that are not consciously selected for rapid development or early reproduction, potentially leading to reduced sexual selection. We show that rapidly developing and early reproducing populations have very low levels of mating in their lifetime (females are more or less monandrous), low courtship levels, shorter copulation duration, and longer time from eclosion to first mating, compared to the controls. These results are discussed in the context of the previously demonstrated reduction of inter-locus sexual conflict in these populations. We show that life-history strategies might have a large and significant impact on sexual selection, with each influencing the other and contributing to the complexities of adaptation.Significance statementSexual conflict, often manifested as an arms-race between males and females trying to enhance their own reproductive success at some cost to the other, is of great evolutionary interest because it can maintain genetic variation in populations, prevent the independent optimization of male and female traits, and also promote speciation. Sexual selection, or variation in mating success, is well known to affect levels of sexual conflict. However, it is not so clear whether, and how, the regular evolution of life-histories also affects sexual selection. Here, we show that life-history evolution in fruit fly populations selected for traits not directly related to sexual conflict might, nevertheless, mediate the possible evolution of altered sexual conflict levels through effects on sexual selection. Populations that evolved to develop to adulthood fast, and reproduce relatively early in life, are shown to potentially experience less sexual selection, which can explain the low sexual conflict levels earlier observed in them.

Female preference for males successful in male-male competition is generally assumed to result in mating with high quality males. Here I report results from an experiment disentangling the effects of intra- and intersexual selection in the sand goby, Pomatoschistus minutus, a marine fish that exhibits paternal care. I show that large males are successful in male–male competition, but contrary to what one would expect, dominants are not preferred by females and are not better at taking care of the eggs. Female preference, however, correlated with the subsequent hatching success of the eggs. Thus, female choice selects for good parenting. Hence, direct benefits in the form of superior paternal care can explain female choice in this species, supporting a good parent process of sexual selection. However, choosing on the outcome of male–male competition does not enable females to mate with the 'best' males.