Intensity Of Sexual Selection Research Articles

Polygamy slows down population divergence in shorebirds.

Sexual selection may act as a promotor of speciation since divergent mate choice and competition for mates can rapidly lead to reproductive isolation. Alternatively, sexual selection may also retard speciation since polygamous individuals can access additional mates by increased breeding dispersal. High breeding dispersal should hence increase gene flow and reduce diversification in polygamous species. Here, we test how polygamy predicts diversification in shorebirds using genetic differentiation and subspecies richness as proxies for population divergence. Examining microsatellite data from 79 populations in 10 plover species (Genus: Charadrius) we found that polygamous species display significantly less genetic structure and weaker isolation‐by‐distance effects than monogamous species. Consistent with this result, a comparative analysis including 136 shorebird species showed significantly fewer subspecies for polygamous than for monogamous species. By contrast, migratory behavior neither predicted genetic differentiation nor subspecies richness. Taken together, our results suggest that dispersal associated with polygamy may facilitate gene flow and limit population divergence. Therefore, intense sexual selection, as occurs in polygamous species, may act as a brake rather than an engine of speciation in shorebirds. We discuss alternative explanations for these results and call for further studies to understand the relationships between sexual selection, dispersal, and diversification.

Himalayan black bulbuls (Hypsipetes leucocephalus niggerimus) exhibit sexual dichromatism under ultraviolet light that is invisible to the human eye

Sexual dichromatism is a key proxy for the intensity of sexual selection. Studies of dichromatism in birds may, however, have underestimated the intensity and complexity of sexual selection because they used museum specimens alone without taking colour-fading into account or only measured conspicuous visual traits in live animals. We investigated whether the Himalayan black bulbul (Hypsipetes leucocephalus nigerrimus), which is sexually monomorphic to the human eye, exhibits sexual dichromatism distinguishable by a spectrometer. We measured the reflectance (within both the human visual perceptive and the ultraviolet ranges) of two carotenoid-based parts and eight dull and melanin-based parts for each individual live bird or museum skin sampled. According to an avian model of colour discrimination thresholds, we found that males exhibited perceptibly redder beaks, brighter tarsi and darker plumage than did females. This suggests the existence of multiple cryptic sexually dichromatic traits within this species. Moreover, we also observed detectable colour fading in the museum skin specimens compared with the live birds, indicating that sexual dichromatism could be underestimated if analysed using skin specimens alone.

Dimorphic male squid show differential gonadal and ejaculate expenditure

Under intense sexual selection, males less successful in fighting and mate guarding often adopt alternative reproductive tactics. In many species, males employing alternative tactics show not only behavioral differences, but also divergences in morphology and physiology, a phenomenon called intrasexual male dimorphism. Herein, we investigated intrasexual male dimorphism in the loliginid squid Doryteuthis plei, associated with alternative mating tactics. We show that small males (sneakers) have spermatophores with discontinuously smaller sperm mass and longer spermatozoa than large males (consorts). Moreover, sneakers produce club-like spermatangia, whereas consorts produce hook-like spermatangia, each type of spermatangia associated with a different female storage site and adoption of a distinct mating position. We also show that dimorphic males have different gonadal investment, sneakers showing higher increment rates in testis mass and higher investment in spermatophoric complex than consorts. Under the complex squid mating system, with two distinct fertilization environments, we hypothesize that sneakers may maximize their reproductive success by both investing more in gonad growth and partitioning ejaculates into extra mating opportunities, whereas consorts may benefit from investment in somatic growth. Squids may be the first example of animals that, even with distinct sperm storage sites, fit the general predictions of sneaks and guards theoretical models.

Sexual selection and sex ratios in Anolis lizards

Biased sex ratios, or unequal numbers of males and females in a population, can alter the intensity of sexual selection by enhancing competition for mates, and thus may affect the evolution of reproductive strategies. Studies of sex ratio variation across a clade provide an opportunity to examine the morphological or behavioral consequences of different levels of sexual selection. We examined sex ratio variation, using phylogenetic comparative methods, across a diverse clade of terrestrial vertebrates, the Anolis lizards. Across a sample of 14 species in 21 localities, we found remarkable bidirectional variation in sex ratios across the Anolis clade: males are more common in some populations and females in others. However, we find no evidence that sex ratio bias is associated with sexual size dimorphism, a proxy for sexual selection. Nor do we find an association of sex ratio bias with ecological niches (i.e. ecomorphs), which vary in sexual selection pressures and mating systems. The observed inter-specific variation in sex ratio suggests that a balance of different, possibly opposing, factors, including sex-specific dispersal and mortality rates, may play a role in determining population sex ratio.

The nature of allometry in an exaggerated trait: The postocular flange in Platyneuromus Weele (Insecta: Megaloptera).

The origin and function of exaggerated traits exhibited by a great number of species with sexual dimorphism remain largely unexplored. The usual model considered as the evolutionary mechanism for the development of these structures is sexual selection. The nature of growth of the postocular flange (POF) in three species of the dobsonfly genus Platyneuromus (Megaloptera, Corydalidae, Corydalinae) is analyzed to explore sexual size dimorphism and allometric scaling. Results involve positive allometry of POF in males of two species, and negative allometry in males of one species, in general with a female-biased sexual dimorphism. We suggest an ancestral condition of dual incipient ornamentation in Platyneuromus, with a subsequent departure of size and shape of POF in males, triggered by sexual selection. Different sexual selection intensities may explain the parallel or divergent growth of POF within the scheme of dual ornamentation. Empirical behavioral data as well as a phylogenetic framework are necessary to clarify possible causes of phenotypic development, time of origin, and evolution of the POF.

Parabolic variation in sexual selection intensity across the range of a cold-water pipefish: implications for susceptibility to climate change.

While an understanding of evolutionary processes in shifting environments is vital in the context of rapid ecological change, one of the most potent selective forces, sexual selection, remains curiously unexplored. Variation in sexual selection across a species range, especially across a gradient of temperature regimes, has the potential to provide a window into the possible impacts of climate change on the evolution of mating patterns. Here, we investigated some of the links between temperature and indicators of sexual selection, using a cold-water pipefish as model. We found that populations differed with respect to body size, length of the breeding season, fecundity, and sexual dimorphism across a wide latitudinal gradient. We encountered two types of latitudinal patterns, either linear, when related to body size, or parabolic in shape when considering variables related to sexual selection intensity, such as sexual dimorphism and reproductive investment. Our results suggest that sexual selection intensity increases toward both edges of the distribution and that the large differences in temperature likely play a significant role. Shorter breeding seasons in the north and reduced periods for gamete production in the south certainly have the potential to alter mating systems, breeding synchrony, and mate monopolization rates. As latitude and water temperature are tightly coupled across the European coasts, the observed patterns in traits related to sexual selection can lead to predictions regarding how sexual selection should change in response to climate change. Based on data from extant populations, we can predict that as the worm pipefish moves northward, a wave of decreasing selection intensity will likely replace the strong sexual selection at the northern range margin. In contrast, the southern populations will be followed by heightened sexual selection, which may exacerbate the problem of local extinction at this retreating boundary.

Feather melanin and microstructure variation in dark‐eyed juncoJunco hyemalisacross an elevational gradient in the Selkirk Mountains

Variation in feather melanism and microstructure can arise through sexual selection and ecological functional drivers. Melanin‐based plumage traits are associated with sexual dichromatism and the intensity of sexual selection in many avian species, but also have several ecological benefits such as protection against ultra‐violet (UV) radiation, camouflage, and feather strength. Additionally, feather microstructure influences thermoregulation. Plumage variation across species is well documented; however, the relative role of sexual selection and ecological drivers in intra‐specific and within‐population variation is less established. We investigated UV reflectance, melanism, and feather microstructure in a population of Oregon dark‐eyed juncosJunco hyemalis oreganusbetween high (1900–2200 m a.s.l.) and low (450–800 m a.s.l.) elevations in the Selkirk Mountains to evaluate potential sexual selection and ecological drivers of variation. We found no difference in UV reflectance or lightness (melanism) of head feathers between elevations, but individuals at high elevation had lighter (less melanism) and less brown (less pheomelanin) body contour feathers than at low elevations. High elevation individuals also had longer contour feathers with more pronounced plumulaceous regions. Sexual dichromatism did not vary between elevations, leading us to reject sexual selection in favour of ecological functional drivers of plumage variation in this system. To our knowledge, this is the first study to identify within‐population differences in feather melanism and microstructure between different elevations.

The effect of colour‐producing mechanisms on plumage sexual dichromatism in passerines and parrots

Summary Sexual dichromatism (SD) often reflects intense sexual selection on males. It has been hypothesized that sexual selection should favour the elaboration of those male colours that honestly signal quality and that such colours should therefore show higher SD. Costliness of colours is expected to vary according to their production mechanism (pigment type, feather microstructure and combinations thereof). Carotenoid‐based colours, due to their dietary origin and competing functions of carotenoid pigments, are the best documented costly colours, while endogenous pigments and structural colours are expected to be less costly. However, how SD varies with colour‐producing mechanism has not been systematically addressed. Here, we test the link between SD and mechanisms of colour production across nearly all Australian passerines (n = 302) and parrots (n = 48), using reflectance spectrometry and visual models. We quantified SD [chromatic (hue and saturation) and achromatic (light to dark)] for individual plumage patches as well as for the whole plumage. We then compared whether these SD estimates vary for plumage produced by different mechanisms of colour production. Not unexpectedly, individual plumage patches were most sexually dichromatic when males and females have different mechanisms of colour production. In most cases however, both sexes share the same mechanism. Among these, red carotenoid‐based plumage in passerines showed the highest SD, while in passerines as well as in parrots, melanin‐based plumage and white plumage have the lowest levels of SD. Average SD within species is weakly predicted by the proportion of the plumage produced by different mechanisms. This effect is strongest for red carotenoids, but equally so for males and females. In contrast, effects of structural and pheomelanin‐based colours are different between sexes, highlighting the links between high SD and the evolution of different mechanisms of colour production in males and females. While our analysis showed that colours based on red carotenoids have higher levels of SD, the differences were small, and most mechanisms of colour production were able to produce a similar range of SD. These results do not support the hypothesis that sexual selection should preferentially lead to the elaboration of some types of colours over others. A lay summary is available for this article.

Devoted fathers or selfish lovers? Conflict between mating effort and parental care in a harem-defending arachnid.

When there is a temporal trade-off between mating effort and parental care, theoretical models predict that intense sexual selection on males leads to reduced paternal care. Thus, high-quality males should invest more in mating effort because they have higher chances of acquiring mates, whereas low-quality males should bias their investment towards parental care. Once paternal care has evolved, offspring value should also influence males' decisions to invest in offspring attendance. Here, we performed a manipulation under field conditions to investigate the factors that influence male allocation in either mating effort or parental care. We predicted that facultative paternal care in the harem-holding harvestman Serracutisoma proximum would be negatively influenced by male attractiveness and positively influenced by offspring value. We found that attractive males were less likely to engage in egg attendance and that the higher the perceived paternity, the higher the caring frequency. Finally, egg mortality was not related to caring frequency by males, but predation pressure was much lower than that recorded in previous studies with the same population. Thus, the benefits of facultative male care may be conditional to temporal variation in the intensity of egg predation. In conclusion, males adjust their investment in either territory defence or egg attendance according to their recent mating history and perceived paternity. Our findings suggest that exclusive paternal care can evolve from facultative paternal care only if the trade-off between mating effort and parental care is circumvented.

Geographical and seasonal variation in the intensity of sexual selection in the barn swallow Hirundo rustica: a meta-analysis.

Sexual selection arises from competition among individuals for access to mates, resulting in the evolution of conspicuous sexually selected traits, especially when inter-sexual competition is mediated by mate choice. Different sexual selection regimes may occur among populations/subspecies within the same species. This is particularly the case when mate choice is based on multiple sexually selected traits. However, empirical evidence supporting this hypothesis at the among-populations level is scarce. We conducted a meta-analysis of the intensity of sexual selection on the largest database to date for a single species, the barn swallow (Hirundo rustica), relying on quantitative estimates of sexual selection. The intensity of sexual selection was expressed as the strength (effect size) of the relationships between six plumage ornaments (tail length, tail asymmetry, size of white spots on tail, ventral plumage colour, throat plumage colour and throat patch size) and several fitness proxies related to reproduction, parental care, offspring quality, arrival date from spring migration, and survival. The data were gathered for four geographically separated subspecies (H. r. rustica, H. r. erythrogaster, H. r. gutturalis, H. r. transitiva). The overall mean effect size (Zr = 0.214; 95% confidence interval = 0.175-0.254; N = 329) was of intermediate magnitude, with intensity of sexual selection being stronger in males than in females. Effect sizes varied during the breeding cycle, being larger before egg deposition, when competition for access to mates reaches its maximum (i.e. in the promiscuous part of the breeding cycle), and decreasing thereafter. In addition, effect sizes from experiments were not significantly larger than those from correlative studies. Finally, sexual selection on different sexually dimorphic traits varied among subspecies. This last result suggests that morphological divergence among populations has partly arisen from divergent sexual selection, which may eventually lead to speciation.

Evolution of the ungulate dewlap: thermoregulation rather than sexual selection or predator deterrence?

BackgroundDewlaps are iconic features of several ungulate species and, although a role in signalling has been postulated, their function remains largely unexplored. We recently failed to find any age-independent link between dewlap size and social status in the common eland (Tragelaphus oryx), pointing to the possibility that sexual selection may not be the primary cause of dewlap evolution in ungulates. Here I use a two-pronged approach to test hypotheses on the function of ungulate dewlaps: an interspecific comparative analysis of bovids and deer, and an intraspecific study of eland antelopes in the wild.ResultsAcross species, the presence of dewlaps in males was not found to be associated with sexual size dimorphism, a commonly used measure of the intensity of sexual selection. The presence of dewlaps was, however, linked to very large male body size (>400 kg), which agrees with a thermoregulatory function as lower surface/volume-ratio counteracts heat dissipation in large-bodied species. In eland antelopes, large dewlap size was associated with higher, rather than lower, incidence of claw-marks (independently of age), a result which speaks against the dewlap as a predator deterrent and rather indicates a predation cost of the structure.ConclusionThe findings suggest that, although an additional function in communication should not be ruled out, the dewlap of ungulates may contrast with that of lizards and birds in thermoregulation being a primary function.

From Evolutionary Allometry to Sexual Display: (A Reply to Holman and Bro-Jørgensen)

Conventional wisdom holds that the complex shapes of deer antlers are produced under the sole influence of sexual selection. We questioned this view by demonstrating that trends for increased body size evolution passively yield more-complex ornaments, even in organisms where no effect of sexual selection is possible, with similar allometric slopes. Recent investigations suggest that sexual selection on antlers of larger deer species is stronger than that in smaller species; hence,the use of conspicuous antlers for display in large male deer is a secondary function driven by especially intense sexual selection on these large-bodied species. Sinceancestral deer were small and had very simple antlers, such an intense selection on antlers shape was probably absent in early deer. Therefore, the evolution of complex ornaments is coupled with body size evolution, even in deer.

Male-biased sex ratio does not promote increased sperm competitiveness in the seed beetle, Callosobruchus maculatus.

Sperm competition risk and intensity can select for adaptations that increase male fertilisation success. Evolutionary responses are examined typically by generating increased strength of sexual selection via direct manipulation of female mating rates (by enforcing monandry or polyandry) or by alteration of adult sex ratios. Despite being a model species for sexual selection research, the effect of sexual selection intensity via adult sex-ratio manipulation on male investment strategies has not been investigated in the seed beetle, Callosobruchus maculatus. We imposed 32 generations of experimental evolution on 10 populations of beetles by manipulating adult sex ratio. Contrary to predictions, males evolving in male-biased populations did not increase their testes and accessory gland size. This absence of divergence in ejaculate investment was also reflected in the fact that males from male-biased populations were not more successful in either preventing females from remating, or in competing directly for fertilisations. These populations already demonstrate divergence in mating behaviour and immunity, suggesting sufficient generations have passed to allow divergence in physiological and behavioural traits. We propose several explanations for the absence of divergence in sperm competitiveness among our populations and the pitfalls of using sex ratio manipulation to assess evolutionary responses to sexual selection intensity.

Sexual selection on male size drives the evolution of male-biased sexual size dimorphism via the prolongation of male development.

Sexual size dimorphism (SSD) arises when the net effects of natural and sexual selection on body size differ between the sexes. Quantitative SSD variation between taxa is common, but directional intraspecific SSD reversals are rare. We combined micro- and macroevolutionary approaches to study geographic SSD variation in closely related black scavenger flies. Common garden experiments revealed stark intra- and interspecific variation: Sepsis biflexuosa is monomorphic across the Holarctic, while S. cynipsea (only in Europe) consistently exhibits female-biased SSD. Interestingly, S. neocynipsea displays contrasting SSD in Europe (females larger) and North America (males larger), a pattern opposite to the geographic reversal in SSD of S. punctum documented in a previous study. In accordance with the differential equilibrium model for the evolution of SSD, the intensity of sexual selection on male size varied between continents (weaker in Europe), whereas fecundity selection on female body size did not. Subsequent comparative analyses of 49 taxa documented at least six independent origins of male-biased SSD in Sepsidae, which is likely caused by sexual selection on male size and mediated by bimaturism. Therefore, reversals in SSD and the associated changes in larval development might be much more common and rapid and less constrained than currently assumed.

How sexual selection can drive the evolution of costly sperm ornamentation.

Post-copulatory sexual selection (PSS), fuelled by female promiscuity, is credited with the rapid evolution of sperm quality traits across diverse taxa. Yet, our understanding of the adaptive significance of sperm ornaments and the cryptic female preferences driving their evolution is extremely limited. Here we review the evolutionary allometry of exaggerated sexual traits (for example, antlers, horns, tail feathers, mandibles and dewlaps), show that the giant sperm of some Drosophila species are possibly the most extreme ornaments in all of nature and demonstrate how their existence challenges theories explaining the intensity of sexual selection, mating-system evolution and the fundamental nature of sex differences. We also combine quantitative genetic analyses of interacting sex-specific traits in D. melanogaster with comparative analyses of the condition dependence of male and female reproductive potential across species with varying ornament size to reveal complex dynamics that may underlie sperm-length evolution. Our results suggest that producing few gigantic sperm evolved by (1) Fisherian runaway selection mediated by genetic correlations between sperm length, the female preference for long sperm and female mating frequency, and (2) longer sperm increasing the indirect benefits to females. Our results also suggest that the developmental integration of sperm quality and quantity renders post-copulatory sexual selection on ejaculates unlikely to treat male-male competition and female choice as discrete processes.

Demographic drivers of age-dependent sexual selection.

Sexual selection has a critical role in evolution, and it is fundamental to identify what ecological factors drive its variation. Disentangling the ecological correlates of sexual selection over the long term, however, is challenging and has rarely been done in nature. We sought to assess how demographic changes influenced the intensity, direction and form of sexual selection and whether selective pressures varied with age. We tested whether breeder sex ratio, number of competitors and age structure influenced selection differentials on horn length of wild bighorn rams (Ovis canadensis) of different age classes on Ram Mountain, Alberta. We used 21years of data including a detailed pedigree, demographic parameters and repeated morphological measurements. Sexual selection on horn length of males of all ages was directional and positive. Selection intensity increased with the number of competitors, reflecting male-male encounter rate during the rut, but was independent of breeder sex ratio or age structure. This result can also be linked to changes in population size because the number of competitors was highly correlated to total number of sheep. This demographic effect likely arises from age-dependent mating tactics. Males aged 2-4years are weakly competitive and experienced stronger sexual selection as they accounted for a greater proportion of all males. Selection experienced by mature males appeared independent of demography. Our study provides a rare description of the demographic determinants of sexual selection in nature.

Sexual selection on skeletal shape in Carnivora.

Lifetime reproductive success of males is often dependent upon the ability to physically compete for mates. However, species variation in social structure leads to differences in the relative importance of intraspecific aggression. Here, we present a large comparative dataset on sexual dimorphism in skeletal shape in Carnivora to test the hypotheses that carnivorans exhibit sexual dimorphism in skeletal anatomy that is reflective of greater specialization for physical aggression in males relative to females and that this dimorphism is associated with the intensity of sexual selection. We tested these hypotheses using a set of functional indices predicted to improve aggressive performance. Our results indicate that skeletal shape dimorphism is widespread within our sample. Functional traits thought to enhance aggressive performance are more pronounced in males. Phylogenetic model selection suggests that the evolution of this dimorphism is driven by sexual selection, with the best-fitting model indicating greater dimorphism in polygynous versus nonpolygynous species. Skeletal shape dimorphism is correlated with body size dimorphism, a common indicator of the intensity of male-male competition, but not with mean body size. These results represent the first evidence of sexual dimorphism in the primary locomotor system of a large sample of mammals.

Sexual selection and assortative mating: an experimental test.

Mate choice and mate competition can both influence the evolution of sexual isolation between populations. Assortative mating may arise if traits and preferences diverge in step, and, alternatively, mate competition may counteract mating preferences and decrease assortative mating. Here, we examine potential assortative mating between populations of Drosophila pseudoobscura that have experimentally evolved under either increased ('polyandry') or decreased ('monogamy') sexual selection intensity for 100 generations. These populations have evolved differences in numerous traits, including a male signal and female preference traits. We use a two males: one female design, allowing both mate choice and competition to influence mating outcomes, to test for assortative mating between our populations. Mating latency shows subtle effects of male and female interactions, with females from the monogamous populations appearing reluctant to mate with males from the polyandrous populations. However, males from the polyandrous populations have a significantly higher probability of mating regardless of the female's population. Our results suggest that if populations differ in the intensity of sexual selection, effects on mate competition may overcome mate choice.

Age-specific survival in the socially monogamous alpine marmot (Marmota marmota): evidence of senescence

We investigated age-specific variation in survival of dominant individuals in a long-lived and monogamous mammal, the alpine marmot ( Marmota marmota ), from a large dataset collected during a 24-year intensive monitoring of a free-ranging population. We found evidence of actuarial senescence in dominant individuals for both sexes. Survivorship was constant with age until dominant marmots were between 6 and 8 years of age and declined markedly thereafter. No between sex differences occurred in the intensity of actuarial senescence, which might be related to the weak intensity of sexual selection in this socially monogamous mammal. More investigations are needed to know whether cooperative breeding, hibernation, and monogamy, which are key features of the alpine marmot life history, could have shaped the patterns of actuarial senescence we report.

Condition dependence of male and female reproductive success: insights from a simultaneous hermaphrodite.

Sexually selected traits are predicted to show condition dependence by capturing the genetic quality of its bearer. In separate-sexed organisms, this will ultimately translate into condition dependence of reproductive success of the sex that experiences sexual selection, which is typically the male. Such condition dependence of reproductive success is predicted to be higher in males than females under conditions promoting intense sexual selection. For simultaneous hermaphrodites, however, sex allocation theory predicts that individuals in poor condition channel relatively more resources into the male sex function at the expense of the female function. Thus, male reproductive success is expected to be less condition dependent than female reproductive success. We subjected individuals of the simultaneously hermaphroditic snail Physa acuta to two feeding treatments to test for condition dependence of male and female reproductive success under varying levels of male-male competition. Condition dependence was found for female, but not for male, reproductive success, meaning that selection on condition is relatively stronger through the female sex function. This effect was consistent over both male-male competition treatments. Decomposition of male and female reproductive performance revealed that individuals in poor condition copulated more in their male role, indicating an increased male allocation to mate acquisition. These findings suggest that sex-specific condition dependence of reproductive success is at least partially driven by condition-dependent sex allocation. We discuss the implications of condition-dependent sex allocation for the evolution of sexually selected traits in simultaneous hermaphrodites.