Mechanisms of species divergence through visual adaptation and sexual selection:Perspectives from a cichlid model system

The theory of ecological speciation suggests that assortative mating evolves most easily when mating preferences aredirectly linked to ecological traits that are subject to divergent selection. Sensory adaptation can play a major role in this process,because selective mating is often mediated by sexual signals: bright colours, complex song, pheromone blends and so on. Whendivergent sensory adaptation affects the perception of such signals, mating patterns may change as an immediate consequence.Alternatively, mating preferences can diverge as a result of indirect effects: assortative mating may be promoted by selectionagainst intermediate phenotypes that are maladapted to their (sensory) environment. For Lake Victoria cichlids, the visual environmentconstitutes an important selective force that is heterogeneous across geographical and water depth gradients. We investigatethe direct and indirect effects of this heterogeneity on the evolution of female preferences for alternative male nuptial colours(red and blue) in the genus Pundamilia. Here, we review the current evidence for divergent sensory drive in this system, extractgeneral principles, and discuss future perspectives [Current Zoology 56 (3): 285-299, 2010].

Sexual selection affects the sizes of the mammalian prostate gland and seminal vesicles

The accessory reproductive glands of male mammals contribute the bulk of the secretions in which spermatozoa are transported to the female tract during copulation. Despite their morphological diversity, and the chemical complexity of their products, little is known about the possible effects of sexual selection upon these glands in mammals. Here we consider the seminal vesicles and prostate glands in a sample of 89 species and 60 genera representing 8 Orders of mammals. The sizes of the accessory glands are analysed in relation to body weight and testes weight. Both the seminal vesicles size and prostate size （corrected for body weight） correlate positively with relative testes size in this sample; this finding remains highly significant after application of procedures to correct for possible phylogenetic biases in the data set. The accessory reproductive glands are also significantly larger in those mammals which have large relative testes sizes, and in which the likelihood of sperm competition is greatest. These results support the hypothesis that sexual selection has played an important role in the evolution of the mammalian prostate gland and seminal vesicles.

The measurement of sexual selection on females and males

As in any field of research, the study of sexual selection is subject to ongoing debate over definitions and interpreta- tions of the fundamental concepts involved. These arguments generally promote progress, as they highlight areas where current explanations are incomplete. Here we briefly review two ongoing discussions in the sexual selection literature. First, the definition of sexual selection has received renewed interest in light of increasing research effort into when and how it operates in females. Second, how best to measure sexual selection is an ongoing subject of debate; in practice, recognition that the appropriate measures depend on the focus of the specific study, and that multiple measures should be employed wherever possible, seems to provide the most informative approach. The wide scope of recent empirical work in these and related areas, with the application of new techniques and approaches, reflects that the field of sexual selection is being constantly expanded and enriched

Mating behavior and sexual selection in a polygamous beetle

Mating behavior and sexual selection in relation to morphometric traits in a polygamous beetle, Glenea cantor （F.） （Coleoptera： Cerambycidae）, were investigated. Upon encounter, a male approached a female, mounted her, grasped her terminal abdomen with his hind tarsi, and attempted to mate. Successful mating lasted about 3.5 h. Although all traits measured in females and half of traits in males were significantly correlated with mating success, the primary selection on virgin females was the genital trait, thebursa copulatrix length, and that on males was the body length and hind tarsal length. Longer bursa copulatrix accommodated a larger ejaculate, suggesting that this female trait benefits the male that first mates with the female in terms of in- creasing ejaculate size to beat subsequent males in sperm competition. Under a female-biased sex ratio, more than 20% of mat- ings failed within 20s after the male genitalia had been inserted into hers, suggesting that males assess genital features of the re- ：male before insemination and undertake cryptic male mate choice. Larger males were more capable of grasping females and achieving mating. During the premating struggle the male almost always used his hind tarsi to lift the female terminal abdomen to the position for his genitalia to insert, and as a result, males with longer hind tarsi achieved higher mating success [Current Zoolo- gy 59 （2）： 257-264, 2013].

Can sexual selection and disassortative mating contribute to the maintenance of a shell color polymorphism in an inter- tidal marine snail？

Littorina fabalis is an intertidal snail commonly living on the brown algae Fucus vesiculosus and showing frequent shell-color polymorphisms in the wild. The evolutionary mechanism underlying this polymorphism is currently unknown. Shell color variation was studied in mated and non-mated specimens of this species from different microareas in one locality from NW Spain, in order to estimate sexual selection and assortative mating that may （still） be operating in this population. The analyses across microareas allowed us to investigate frequency-dependent selection and assortative mating components, mechanisms that could maintain the polymorphism. The presence of shell scars caused by crab attacks, an environmental variable not related with sexual selection or assortative mating, was used as experimental control. This study provides new evidence of significant disas- sortative mating and some degree of sexual selection against some shell colors, supporting the results found 21 years ago in a similar study, i.e. in the same species and locality. The similarity of these estimates during the studied period suggests that this experimental approach is consistent and valid to be extended to other populations and organisms. In addition, sexual selection and assortative mating estimates did not change across microareas differing in shell color frequencies, suggesting than the polymor- phism can not be maintained by a frequency-dependent （sexual selection-based） mechanism. Our main hypothesis is that negative assortative mating could contribute to the maintenance of the polymorphism, perhaps by males showing distinct female color preferences when searching for mates [Current Zoology 58 （3）： 463-474, 2012].

The roles of inter- and intra-sexual selection in behavioral isolation between native and invasive pupfishes

Male-male competition and female mate choice may both play important roles in driving and maintaining reproductive isolation between species. When previously allopatric species come into secondary contact with each other due to introductions, they provide an opportunity to evaluate the identity and strength of reproductive isolating mechanisms. If reproductive isolation is not maintained, hybridization may occur. We examined how reproductive isolating mechanisms medi- ate hybridization between endemic populations of the Red River pupfish Cyprinodon rubrofluviati- lis and the recently introduced sheepshead minnow C. variegatus. In lab-based dominance trials, males of both species won the same number of competitions. However, male C. rubrofluviatilis that won competitions were more aggressive than C, variegatus winners, and more aggression was needed to win against competitor C. variagatus than allopatric C. rubrofluviatilis. Duration of fights also differed based on the relatedness of the competitor. In dichotomous mate choice trials, there were no conspecific or heterospecific preferences expressed by females of either species. Our findings that male-male aggression differs between closely and distantly related groups, but female choice does not suggest that male-male competition may be the more likely mechanism to impede gene flow in this system.

Sexual selection for bright females prevails under light pollution

The functions of sexually selected traits are particularly sensitive to changes in the environment because the traits have evolved to increase mating success under local environmental conditions(Rosenthal and Stuart-Fox 2012).When environmental conditions change,previously reliable signals may become less reliable or harder to detect and evaluate.Because the correct expression,transmission,and interpretation of sexual signals typically influence mate choice outcomes,impediments to sexual signals can change both the strength and the direction of sexual selection(Rosenthal and Stuart-Fox 2012).Artificial light is a major anthropogenic disturbance that is intensifying around the world and has high potential to negatively impact wildlife,for example by hampering the expression and detection of sexual signals.

The importance of pre-and postcopulatory sexual selection promoting adaptation to increasing temperatures

Global temperatures are increasing rapidly affecting species globally.Understanding if and how different species can adapt fast enough to keep up with increasing temperatures is of vital importance.One mechanism that can accelerate adaptation and promote evolutionary rescue is sexual selection.Two different mechanisms by which sexual selection can facilitate adaptation are pre-and postcopulatory sexual selection.However,the relative effects of these different forms of sexual selection in promoting adaptation are unknown.Here,we present the results from an experimental study in which we exposed fruit flies Drosophila melanogaster to either no mate choice or 1 of 2 different sexual selection regimes(pre-and postcopulatory sexual selection)for 6 generations,under different thermal regimes.Populations showed evidence of thermal adaptation under preco-pulatory sexual selection,but this effect was not detected in the postcopulatory sexual selection and the no choice mating regime.We further demonstrate that sexual dimorphism decreased when flies evolved under increasing temperatures,consistent with recent theory predicting more sexually concordant selection under environmental stress.Our results suggest an important role for precopulatory sexual selection in promoting thermal adaptation and evolutionary rescue.

Sexual selection on color and behavior within and between cichlid populations： Implications for speciation

Sexual selection is widely viewed as playing a central role in haplochromine cichlid speciation. Hypothetically, once divergent mate preferences evolve among populations of these fishes, reproductive isolation follows and the populations begin to behave as different species. Various studies have examined patterns of assortative mating among species and sometimes populations, but few have examined variation in directional preferences, especially among populations of the same species. We investi- gated mate choice behavior in two populations of Labeotropheus fueUeborni, a Lake Malawi endemic. We test whether mating preferences between populations are based on the same traits and in the same direction as preferences within populations. We examine the potential contributions of two classes of trait, color patterns and behaviors, to reproductive isolation. When females chose between either two males of their own population, or two from another, female preferences were generally similar （for the female population） across the two contexts. Mate choice patterns differed between （female） populations for a measure of color, but only modestly for male behavior. In a separate experiment we simultaneously offered females a male of their own population and a male from a different population. In these trials, females consistently preferred males from their own population, which were also the males that displayed more frequently than their opponents, but not necessarily those with color traits suggested to be most attractive in the previous experiment. Thus directional preferences for chroma and related aspects of color may be important when females are presented with males of otherwise similar phenotypes, but may play little role in mediating assortative mating among populations with substantially different color patterns. A preference for male behavior could play some role in speciation if males preferentially court same-population females, as we have observed for the populations studied herein [Current Zoology 58 （3）： 475-483, 2012].

Sexual selection and hermaphroditic organisms： Testing theory

Sexual selection is widespread if not ubiquitous in hermaphroditic organisms. Although many phenomena that have been described as sexual selection in gonochores, （e.g. harem polygamy, multiple mating, elaborate courtship, even secondary sexual characters） can be found in some hermaphrodites, what is more interesting is the ways in which sexual selection in her- maphrodites may differ from dioecious taxa. In hermaphrodites, an individual＇s mating success includes its success from both sexual roles. Secondly, in many simultaneously hermaphroditic taxa there is strong evidence of sexual selection and yet the ope- rational sex ratio is 1：1, by definition. Many simultaneous hermaphrodites have elaborate courtship and genital anatomy, suggest- ing sexual selection plays an important role in reproductive success. Sperm competition and cryptic female choice mean that the number of mates acquired is not necessarily a predictor of reproductive success. Even in simultaneous hermaphrodites with re- ciprocal mating, variance in reproductive success through the male role and through the female role may differ in a population. Moreover hermaphrodites may choose to emphasize one sexual role over the other. Data suggest that the preferred role varies in hermaphrodites, which creates an opportunity to test fundamental predictions and assumptions of sexual selection theory. Hermaphrodites may vary their emphasis on one sexual role over the other either developmentally or behaviorally in response to environmental or social parameters. How they use this capability in acquiring more or higher quality mates still requires study

Sexual selection and incipient speciation in Hawaiian Drosophila

We conducted sexual selection experiments to produce strains with high and low mating discrimination in females of laboratory strains of Hawaiian Drosophila, D.silvestris, then examined secondary sexual traits of these two lines, and compared them with that of standard line. In order to do this, we screened out super-males which mated successfully with females and with high mating records;and poor males which usually could not mate successfully with females and had low mating records. In the meantime,choosy females were also screened out, which almost never responded to males' nuptial dance and were difficult to be mated; but indiscriminate females were on the contrary,which were very ready to accept male's nuptial dance and were very easy to be mated. As a result, by mating supermales with choosy females, we were able to produce the high-line strain; similarly, for the low line, we mated poor males with indiscriminate females and we had a strain that was significantly different from our standard strain within just two generations of selection, i.e., morphological trait differences were measured between the standard strain and the two selected lines, which indicated that mating discrimination has affected secondary sexual traits of the lowline strain significantly: Cilia number on the foretibia of low-line males is significantly different from that of the standard line, which perhaps was the indication of incipient speciation in Hawaiian Drosophila.

When sexual selection in hosts benefits parasites

In host-parasite coevolution,the parasite is selected to increase its infectivity while host is selected to resist the parasite infection.It is widely held that parasite-mediated sexual selection can further amplify the selective pressure on the host to overcome parasite infection.In this paper we focus on certain types of parasites,those that can impair the activity of the host immune function to prevent signs of sickness.We show that the effect of sexual selection can actually reduce the selective pressure on the host immune response to adapt to the parasite infection.We design a simple mathematical model for a population of sexually reproducing organism in which individuals are choosy,preferring traits that are correlated negatively with immune system activity.We introduce to this population a parasite that can suppress activation of the host's immune response.Our results show that even though the host immune system is likely to ultimately evolve and adapt to the parasite infection,when sexual selection is part of this process,it can slow down this evolution on the host and give the parasite more time to get established.

No evidence for a genetic association between female mating preference and male secondary sexual trait in a Lake Victoria cichlid fish

Sexual selection by female mating preference for male nuptial coloration has been suggested as a driving force in the rapid speciation of Lake Victoria cichlid fish. This process could have been facilitated or accelerated by genetic associations between female preference loci and male coloration loci. Preferences, as well as coloration, are heritable traits and are probably determined by more than one gene. However, little is known about potential genetic associations between these traits. In turbid water, we found a population that is variable in male nuptial coloration from blue to yellow to red. Males at the extreme ends of the phenotype distribution resemble a reproductively isolated species pair in clear water that has diverged into one species with blue-grey males and one species with bright red males. Females of the turbid water population vary in mating preference coinciding with the male phenotype distribution. For the current study, these females were mated to blue males. We measured the coloration of the sires and male offspring. Parents-offspring regression showed that the sires did not affect male offspring coloration, which confirms earlier findings that the blue species breeds true. In contrast, male offspring coloration was determined by the identity of the dams, which suggests that there is heritable variation in male color genes between females. However, we found that mating preferences of the dams were not correlated with male offspring coloration. Thus, there is no evidence for strong genetic linkage between mating preference and the preferred trait in this population [Current Zoology 56 （1）： 57-64 2010].

Coevolution of Male and Female Response Preferences to Sexual Signals in Music Frogs

Male signaling influences both female choice and male-male competition. Although male signaling characteristics and female preferences have been shown to coevolve in many species, few studies have examined whether male signal characteristics and male receiver responses related to male-male competition also coevolve. The present study tested the hypothesis that male and female signal receiver preferences may coevolve in parallel for flogs in the genus Babina by comparing the acoustic structure of male advertisement calls of four closely related and geographically isolated Babina species. Then we assessed the behavioral responses of both male and female B. daunchina （Emei music frog） to male call playbacks from each of the four species. The results support the hypothesis that male and female signal receiver preferences have coevolved in this species. Specifically, both male and female B. daunchina respond strongly to the heterospecific calls of B. hainanensis, suggesting that preexisting biases exist in both females and males. Both male and female individuals showed a slight response to the calls of B. adenopleura while no response was evoked by the calls ofB. lini. The manifestation of similar response profiles in male and female B. daunchina to the calls of the four species support the idea that male and female signal receiver preferences evolved in parallel and that the origin of these receiver biases reflects adaptations dependent on the same neural and cognitive systems in both sexes.

Sexual Dimorphism in the Hindlimb Muscles of the Asiatic Toad(Bufo gargarizans)in Relation to Male Reproductive Success

In many anurans, the forelimb muscles of males are used to grasp females and are often heavier than those of females despite the larger female body size. Such sexual dimorphism in forelimb musculature is thought to result from sexual selection. In addition, the hindlimbs of frogs and toads play an important role in the reproductive process as amplectant males can expel rivals with robust hindlimbs through kicking. In this study, the sexual dimorphism in dry mass for six hindlimb muscles of the Asiatic toad （Bufo gargarizans） was investigated. The results showed that, when controlled for body size, the hindlimb muscle mass of males significantly exceeded that of females for every muscle. The hindlimb muscle mass of amplectant males was also significantly larger than that of non-amplectant males. These results suggested that if strong hindlimb muscles could improve mating success of males, sexual selection would promote the evolution of dimorphism in this character.

Female waist-to-hip ratio,body mass index and sexual attractiveness in China

Men and women at Northwest University （n=751）, Xi＇an, China were asked to judge the attractiveness of photographs of female patients who had undergone micrograft surgery to reduce their waist-to-hip ratios （WHR）. Micrograft surgery involves harvesting adipose tissue from the waist and reshaping the buttocks to produce a low WHR and an ‘hourglass＇ female figure. This gynoid distribution of female body fat has been shown to correlate with measures of fertility and health. Significantly larger numbers of subjects, of both sexes, chose post-operative photographs, with lower WHRs, as more attractive than pre-operative photographs of the same women. Some patients had gained, and some had lost weight, post-operatively, with resultant changes in body mass index （BMI）. However, these changes in BMI were not related to judgments of attractiveness. These results show that the hourglass female figure is rated as attractive in China, and that WHR, rather than BMI, plays a crucial role in such attractiveness judgments.

Effect of Female Reproduction and Mate Choice on Sexual Size Dimorphism in the Northeast Treefrog Hyla ussuriensis (Anura:Hylidae) in China

Sexual size dimorphism(SSD) plays a significant role in understanding the evolution of life history and mating behavior. In this study,we analyzed the morphological data from a treefrog,Hyla ussuriensis,in northeastern China and found that there are significant differences between males and females. Females that are larger in body size increase fecundity as the total number of eggs is positively correlated to female body size. Males are smaller in body size due to the mate choice by females based on the size dimorphism index(SVL mean of female divided by that of male) for the population,which may be an evolutionary stable strategy(ESS). SSD can be influenced not only through mate choice,but also reproductive behavior by analyzing the female reproduction output in the field. Our data are consistent with many previous studies,indicating that fecundity selection and sexual selection may be the common cause for sexual dimorphism in this species. Furthermore,there are no significant morphological differences between mated and unmated frogs of both sexes,which suggests that any frog can obtain a breeding chance when it matures. It further indicates that males may not affect female choice except by their snout-vent length(SVL) and body mass. It is,of course,possible that females adopt a mating strategy to mate with males whose SVL and body mass are smaller than paired females. Our research provides unequivocal evidence for effective female choice and information on the evolution of SSD in the production of anuran pairing patterns.

Sexual dichromatism and assortative mating by multiple plumage color traits in wild Chestnut Thrush

Sex differences in plumage color are common in bird species.Some bird species are regarded as sexually monochromatic in human visual systems,and in recent years,some species are found to be of cryptic(to human)sexual dichromatism by spectrophotometric techniques.However,the functions of plumage color are still less understood in these species.Here,we focused on plumage color traits in the Chestnut Thrush(Turdus rubrocanus),which is considered as a sexually monochromatic bird by human observers.We used spectrometer analyses and avian visual modeling to investigate the color traits of males and females,and whether these color traits are involved in assortative mating.We found that Chestnut Thrush showed sexual dichromatism in bill,throat and wing,and pairs mated assortatively with colorations of throat,chest,crown and wing.We also found that color of tarsus was different between two consecutive years.These results revealed that Chestnut Thrush is sexually dichromatic in the avian visual system,and plumage color traits play important roles in mate choice.

Sexual Dimorphism in Mass of the Hindlimb Muscles of the Piebald Odorous Frog(Odorrana schmackeri)

Male-biased sexual dimorphism in hind limb muscles is widespread in anuran species where scramble competition is common among males. Such sexual difference is thought to result from sexual selection. In this view, we tested the differences in muscle mass between the sexes and between amplectant and non-amplectant males by quantifying the mass of four hindlimb muscles （triceps femoris, sartorius, gracilis and plantaris longus） of females and males of Odorrana schmackeri. The results showed that females significantly exceeded males for muscle triceps femoris, gracilis, plantaris longus and total mass when controlled for body size. There are no significant differences between amplectant and non-amplectant males. It is probable that the maintenance of the amplectant position in O. schmackeri may depend on the strength of hindlimb muscles in females to support the pair.

A novel method to collect sperm from brood parasitic cuckoos:Urodeum stimulation(UroS)method

Sperm competition has been studied in numerous species as a representative example of postcopulatory sexual selection,where sampling sperm from male is the most basic and important step.Sperm collection can be tricky in birds,however,because unlike mammals,the genitals of birds are generally latent in the cloacal region and their characteristics vary among species.Various methods to collect sperm from different birds have been tested,such as cloacal massage,feces collection,and electro-stimulation,but their applicability varies depending on species.In this study,we introduced the urodeum stimulation method(UroS method)to collect sperm from Cuculus cuckoos,such as the Common Cuckoo(C.canorus).These species are expected to have interesting patterns of pair bonding and sperm competition because of their unique breeding strategy called brood parasitism;however,it remains unexplored.In this study,we described the application of our new method to expel semen from male common cuckoos,measured the volume of semen collected,checked the presence of sperm in the semen sample,and finally estimated its success rate among 82 males.Samples were successfully collected from 76 cuckoos(approximately 93%)and the colors and volumes of the samples were very diverse.Sperm was present in 43 of these samples(57%),showing a sperm observation rate approximately twice as high as that of the conventional cloacal massage method.We believe that this novel method will contribute to a better understanding of postcopulatory sexual selection in avian brood parasites and facilitate the process of sperm collection and artificial insemination in other medium-sized birds.