Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps

Sexual dimorphism is typically a result of strong sexual selection on male traits used in male–male competition and subsequent female choice. However, in social species where reproduction is monopolized by one or a few individuals in a group, selection on secondary sexual characteristics may be strong in both sexes. Indeed, sexual dimorphism is reduced in many cooperatively breeding vertebrates and eusocial insects with totipotent workers, presumably because of increased selection on female traits. Here, we examined the relationship between sexual dimorphism and sociality in eight species of Synalpheus snapping shrimps that vary in social structure and degree of reproductive skew. In species where reproduction was shared more equitably, most members of both sexes were physiologically capable of breeding. However, in species where reproduction was monopolized by a single individual, a large proportion of females—but not males—were reproductively inactive, suggesting stronger reproductive suppression and conflict among females. Moreover, as skew increased across species, proportional size of the major chela—the primary antagonistic weapon in snapping shrimps—increased among females and sexual dimorphism in major chela size declined. Thus, as reproductive skew increases among Synalpheus, female–female competition over reproduction appears to increase, resulting in decreased sexual dimorphism in weapon size.     

A Nonsense Mutation in TMEM95 Encoding a Nondescript Transmembrane Protein Causes Idiopathic Male Subfertility in Cattle

Genetic variants underlying reduced male reproductive performance have been identified in humans and model organisms, most of them compromising semen quality. Occasionally, male fertility is severely compromised although semen analysis remains without any apparent pathological findings (i.e., idiopathic subfertility). Artificial insemination (AI) in most cattle populations requires close examination of all ejaculates before insemination. Although anomalous ejaculates are rejected, insemination success varies considerably among AI bulls. In an attempt to identify genetic causes of such variation, we undertook a genome-wide association study (GWAS). Imputed genotypes of 652,856 SNPs were available for 7962 AI bulls of the Fleckvieh (FV) population. Male reproductive ability (MRA) was assessed based on 15.3 million artificial inseminations. The GWAS uncovered a strong association signal on bovine chromosome 19 (P = 4.08×10⁻⁵⁹). Subsequent autozygosity mapping revealed a common 1386 kb segment of extended homozygosity in 40 bulls with exceptionally poor reproductive performance. Only 1.7% of 35,671 inseminations with semen samples of those bulls were successful. None of the bulls with normal reproductive performance was homozygous, indicating recessive inheritance. Exploiting whole-genome re-sequencing data of 43 animals revealed a candidate causal nonsense mutation (rs378652941, c.483C>A, p.Cys161X) in the transmembrane protein 95 encoding gene TMEM95 which was subsequently validated in 1990 AI bulls. Immunohistochemical investigations evidenced that TMEM95 is located at the surface of spermatozoa of fertile animals whereas it is absent in spermatozoa of subfertile animals. These findings imply that integrity of TMEM95 is required for an undisturbed fertilisation. Our results demonstrate that deficiency of TMEM95 severely compromises male reproductive performance in cattle and reveal for the first time a phenotypic effect associated with genomic variation in TMEM95.     

Polymorphism of growth hormone gene and its association with seminal and sexual behavioral traits in crossbred cattle

The decline in the male reproductive ability in terms of sexual behavior and seminal traits might lead to nonavailability of required number of bulls in a progeny testing program. The present study was conducted in 493 crossbred cattle (Bos taurus × Bos indicus) bulls to study polymorphisms of growth hormone (GH) gene and its association with seminal and sexual behavioral characteristics. A 428-base pair fragment of GH gene spanning over the fourth exon, fourth intron, and fifth exon was amplified and digested with AluI restriction enzyme. Bulls were found to be polymorphic, with two variants, LL and LV, and higher genotypic frequency for LL being 0.88. Twelve nucleotide changes and a single nonsynonymous substitution of Leucine by Valine were observed from GH1 (L) to GH2 (V). Statistical analysis revealed that the genotype of the GH gene had a significant effect on libido score, reaction time, Flehmen response, requirement of mounting stimulus, sperm mass activity, number of semen doses per collection, individual fresh sperm motility, postthaw sperm motility, acrosome integrity, hypo-osmotic swelling test, live and dead count, total morphological abnormality, and head abnormality of sperm in crossbred bulls. Growth hormone gene might be considered a candidate gene for seminal and sexual behavioral traits in crossbred cattle.     

Sexual Experience Enhances Drosophila melanogaster Male Mating Behavior and Success

Competition for mates is a wide-spread phenomenon affecting individual reproductive success. The ability of animals to adjust their behaviors in response to changing social environment is important and well documented. Drosophila melanogaster males compete with one another for matings with females and modify their reproductive behaviors based on prior social interactions. However, it remains to be determined how male social experience that culminates in mating with a female impacts subsequent male reproductive behaviors and mating success. Here we show that sexual experience enhances future mating success. Previously mated D. melanogaster males adjust their courtship behaviors and out-compete sexually inexperienced males for copulations. Interestingly, courtship experience alone is not sufficient in providing this competitive advantage, indicating that copulation plays a role in reinforcing this social learning. We also show that females use their sense of hearing to preferentially mate with experienced males when given a choice. Our results demonstrate the ability of previously mated males to learn from their positive sexual experiences and adjust their behaviors to gain a mating advantage. These experienced-based changes in behavior reveal strategies that animals likely use to increase their fecundity in natural competitive environments.     

Possible Secondary Population-Level Effects of Selective Harvest of Adult Male Muskoxen

Selective harvest regimes are often focused on males resulting in skewed sex-ratios, and for many ungulate species this strategy is sustainable. However, muskoxen (Ovibos moschatus) are very social and mature bulls (≥4 years old), particularly prime-age bulls (6–10 years old), play important roles in predator defense and recruitment. A year-round social structure incorporating large males into mixed-sex groups could make this species more susceptible to the effects of selective harvest if population composition and sex-ratios influence overall survival and reproductive success. Using detailed data collected on the muskox population occupying the Seward Peninsula, Alaska during 2002–2012, we formulated the hypothesis that the selective harvest of mature bulls may be related to documented changes in population composition and growth rates in this species. In addition, we reviewed existing published information from two other populations in Alaska, the Cape Thompson and Northeastern populations, to compare population growth rates among the three areas under differential harvest rates relative to our hypothesis. We found that on the Seward Peninsula, mature bull:adult cow ratios declined 4–12%/year and short-yearling:adult cow ratios (i.e., recruitment) declined 8–9%/year in the most heavily harvested areas. Growth rates in all 3 populations decreased disproportionately after increases in the number of bulls harvested, and calf:cow ratios declined in the Northeastern population as harvest increased. While lack of appropriate data prevented us from excluding other potential causes such as density dependent effects and changes in predator densities, our results did align with our hypothesis, suggesting that in the interest of conservation, harvest of mature males should be restricted until causal factors can be more definitively identified. If confirmed by additional research, our findings would have important implications for harvest management and conservation of muskoxen and other ungulate species with similar life-histories.     

Spatial and temporal components of the mating systems of kudu bulls and red deer stags

Observations were made on greater kudu (Tragelaphus strepsiceros) in the Kruger National Park in South Africa. Data on movement patterns, courtship, dominance interactions and proportion of time spent in various activities by males during the breeding season are presented. Comparative data on the apportionment of time by red deer (Cervus elaphus) setages were obtained on the Isle of Rhum, Scotland. While spatial components of male reproductive behaviour were similar in the two species, time-investments differed markedly. Kudu bulls showed little change in time spent feeding and moving during the breeding season, did not herd females and tolerated the presence of younger males. In contrast, red deer stags almost ceased feeding and greatly increased their time spent moving and in sexual or dominance-related activities. Thus the spatial and temporal components of male mating strategies can vary independently and require separate evolutionary explanaions. Comparative data for other ungulates are sparse, but suggest that time-investments are influenced by the duration of the breeding season and the breeding sex ratio. However, kudu bulls incur high mortality costs despite their low time-investments in reproductive activities.     

Sexual segregation by Masai giraffes at two spatial scales

In this paper alternative explanations for observed patterns of sexual segregation by giraffes are examined at two spatial scales: within-habitats and within-landscape. Habitats are defined as recognizable plant associations and the landscape as the collection of all available habitat types. The study was conducted in Mikumi National Park, Tanzania. At the within-landscape level, all sex and age classes of giraffes exhibited high degrees of preference for riverine habitats. Sex differences in habitat selection were mostly due to females with young, who tended to select open floodplain habitats in which their vigilance time was lowest. Males, and females without young, preferred more heavily-wooded habitat. Habitat preferences were not related to observed habitat-specific forage intake rates for either males or females. Within habitats, male and female giraffes selected different feeding heights, males feeding higher in the canopy than females. Females showed a strong tendency to generalize with respect to feeding height. It is suggested that a sexual dimorphism–body size hypothesis provides a parsimonious explanation for the observed feeding height selection patterns, whereas a reproductive strategy hypothesis can explain sex-differences in habitat selection patterns within the landscape.     

Fitness consequences of divorce in the azure-winged magpie depends on the breeding experience of a new mate

Sexual conflict in producing and raising offspring is a critical issue in evolutionary ecology research.Individual experience affects their breeding performance,as measured by such traits of provisioning of offspring and engagement in extra-pair copulations,and may cause an imbalance in sexual conflict.Thus,divorce is hypothesized to occur within aged social pairs,irrespective of current reproductive success.This concept was explored in the azure-winged magpie Cyanopica cyanus by investigating the divorce of a social pair and its relationship to their changes in breeding performance with prior experience.Females engaging in extra-pair copulation may intensify sexual conflicts and may be the main reason for divorce.Once divorced,females repairing with an inexperienced male realized higher reproductive success than that repairing with an experienced male;males repairing with an experienced female realized higher reproductive success than that repairing with an inexperienced female.This finding indicates that the fitness consequence of divorce depends on the breeding experience of new mates.Divorced females can obtain more extra-pair copulations,whereas divorced males cannot,when they repair with inexperienced breeders.Divorced females provisioned a brood at lower rates than inexperienced females whereas divorced males had no such difference.It appears that divorced females can obtain an advantage in sexual conflicts with inexperienced mates in future reproduction.Consequently,females are probably more active than males in divorcing their aged mates so as to select an inexperienced male as a new mate.Azure-winged magpies thus provide novel insights into the implicaticns of sexual conflict in birds.     

Reproductive synchronization in squirrel monkeys (Saimiri)

Groups of squirrel monkeys (Saimiri) that are exposed to certain seasonal environmental stimuli experience a yearly reproductive cycle with discrete mating and birth seasons. Seasonal rainfall or some rainfall induced seasonal changes (such as changes in vegetation or insect fauna) appear to be responsible for timing theSaimiri reproductive cycle. Animals of both sexes show significant physiological and behavioral changes during the yearly cycle. Whether the environmental timing factors affect both the males and the females equally, or affect only one sex directly and the other sex indirectly through social communication is not clear. Three mechanisms by which the reproductive activity of both males and females could be synchronized are presented, and data from a laboratory study and a field study relevant to each mechanism are presented. Several social interaction patterns frequently observed in the field study suggest that (1) male sexual activity may excite female sexual activity through male penile display and/or other stereotyped interactions and/or (2) female sexual activity may excite male sexual activity through pheromone and/or other communication channels.     

Sonomorphology of the reproductive tract in male and pregnant and non-pregnant female Rothschild's giraffes (Giraffa camelopardalis rotschildi)

The application of real-time-B-mode ultrasonography to wild and zoo animal medicine has been shown to improve the understanding of reproductive physiology in many species. Ultrasound technology is especially helpful for monitoring urogenital health, which in turn has advantages for giraffe breeding and welfare in captivity.This study aimed to ultrasonographically describe the genital organs of reproductively healthy male and female giraffes. Through the use of a restrainer, repeated rectal ultrasound examinations were performed over a 2 year period in 2.6 Rothschild's giraffes. Changes in ovarian activity were monitored throughout four different reproductive stages in the females and included immature, mature-cycling, pregnancy, post-partum-period. In the immature giraffes the ovaries showed multiple follicles of which larger ones luteinized to form pseudo-corpora lutea. By comparison, in the mature giraffes the dominant follicle reached an ovulatory diameter of 18.5 ± 0.89 mm. After ovulation, a single corpus luteum rapidly formed and reached a maximum diameter of 33.0 ± 2.4 mm on average. Pregnancy was detected for the first time by the embryonic vesicle, visualized around 28 days post copulation. Follicular development remained ongoing during early pregnancy. In the males, as in other ruminants, the bulbourethral glands and the seminal vesicles were prominent, whereas the prostate gland was indistinct.Knowledge about the reproductive tract morphology and physiology is necessary for diagnosing medical disorders and abnormalities in giraffes. The aim of this study was to help consolidate the current knowledge on basic reproductive parameters for this species.     

Influence of season of birth on growth and reproductive development of Brahman bulls

Seasonal effects on reproduction are more dramatic in Bos indicus than Bos taurus cattle. This experiment evaluated reproductive development of fall- (n=7) versus spring- (n = 10) born Brahman bulls to determine if season of birth affects reproductive development. Measurements of growth and reproductive development began after weaning and continued at bi-weekly intervals until each bull reached sexual maturity. Different stages of sexual development were classified according to characteristics of the ejaculate and included first sperm in the ejaculate, puberty (> 50 x 10(6) sperm/ejaculate), and sexual maturity (two ejaculates with > 500 = 10(6) sperm/ejaculate). Average daily increases in all measured traits were similar in fall- and spring-born bulls and there were no differences in age, body weight, scrotal circumference, or paired testis volume between groups at first sperm or puberty. However, fall-born bulls were older (P < 0.05) than spring-born bulls at sexual maturity (553 days versus 481 days, respectively) as the interval between puberty and sexual maturity was longer (P < 0.05) in fall- than in spring-born bulls (82 days versus 54 days, respectively). The prolonged interval between puberty and sexual maturity in fall-born calves coincided with a short photoperiod (winter) whereas the short interval between puberty and sexual maturity in spring-born calves coincided with a long photoperiod (summer). In conclusion, season of birth affected sexual development; photoperiod might be involved in regulating testicular function immediately after puberty in Brahman bulls.     

Social and demographic influences on the feeding ecology of giraffe in the Luangwa Valley,Zambia: 1973–2014

Body size influences metabolic rate, which impacts feeding ecology. Body mass differs by sex in size‐dimorphic species, such as giraffes, and also by age. Giraffes reside in a fission–fusion social system, which influences feeding ecology due to frequent changes in group size and composition. We analysed 40 years of feeding records collected from a population of Thornicroft's giraffes (Giraffa camelopardalis thornicrofti) living in the Luangwa Valley, Zambia. We examined the influence of herd composition, age and sex on diet. Solitary males and herd males did not differ in diet. Dietary diversity was comparable for females and males, with sex differences in plant species eaten present during the dry season. Age differences in feeding ecology were pronounced, with juveniles often feeding on bushes and smaller trees, while adults tended to feed upon taller trees. Both sexes have evolved foraging strategies that maximize nutrient and energy intake commensurate with their reproductive strategies, with male metabolic requirements sometimes greater, and sometimes less, than that of females. We propose that females are not exchanging foraging efficiency with reproductive tactics by feeding on smaller trees in the open, but are increasing prospects for their calves to survive when confronted with interspecific competition by browsers.     

Post-insemination selection dominates pre-insemination selection in driving rapid evolution of male competitive ability

Sexual reproduction is a complex process that contributes to differences between the sexes and divergence between species. From a male’s perspective, sexual selection can optimize reproductive success by acting on the variance in mating success (pre-insemination selection) as well as the variance in fertilization success (post-insemination selection). The balance between pre- and post-insemination selection has not yet been investigated using a strong hypothesis-testing framework that directly quantifies the effects of post-insemination selection on the evolution of reproductive success. Here we use experimental evolution of a uniquely engineered genetic system that allows sperm production to be turned off and on in obligate male-female populations of Caenorhabditis elegans. We show that enhanced post-insemination competition increases the efficacy of selection and surpasses pre-insemination sexual selection in driving a polygenic response in male reproductive success. We find that after 10 selective events occurring over 30 generations post-insemination selection increased male reproductive success by an average of 5- to 7-fold. Contrary to expectation, enhanced pre-insemination competition hindered selection and slowed the rate of evolution. Furthermore, we found that post-insemination selection resulted in a strong polygenic response at the whole-genome level. Our results demonstrate that post-insemination sexual selection plays a critical role in the rapid optimization of male reproductive fitness. Therefore, explicit consideration should be given to post-insemination dynamics when considering the population effects of sexual selection.     

It takes two to tango: reproductive skew and social correlates of male mating success in a lek-breeding bird

Variance in reproductive success among individuals is a defining characteristic of many social vertebrates. Yet, our understanding of which male attributes contribute to reproductive success is still fragmentary in most cases. Male–male reproductive coalitions, where males jointly display to attract females, are of particular interest to evolutionary biologists because one male appears to forego reproduction to assist the social partner. By examining the relationship between social behaviour and reproductive success, we can elucidate the proximate function of coalitions in the context of mate choice. Here, we use data from a 4-year study of wire-tailed manakins (Pipra filicauda) to provide molecular estimates of reproductive skew and to test the hypothesis that male–male social interactions, in the context of coordinated displays, positively influence a male''s reproductive success. More specifically, we quantify male–male social interactions using network metrics and predict that greater connectivity will result in higher relative reproductive success. Our data show that four out of six leks studied had significant reproductive skew, with success apportioned to very few individuals in each lek. Metrics of male social affiliations derived from our network analysis, especially male connectivity, measured as the number of males with whom the focal male has extended interactions, were strong predictors of the number of offspring sired. Thus, network connectivity is associated with male fitness in wire-tailed manakins. This pattern may be the result of shared cues used by both sexes to assess male quality, or the result of strict female choice for coordinated display behaviour.     

A sexual selection model for hominid evolution

The following paper develops a sexual selection model for the evolution of bipedal locomotion, canine reduction, brain enlargement, language and higher intelligence. The model involves an expansion of Darwin’s ideas about human evolution based on recent elaborations of sexual selection theory. Modern notions about intrasexual competition and female and male choice and their ecological correlates are summarized along with a new model for the role of sexual selection in speciation. Rapid evolution of bipedal locomotion as a male adaptation for nuptial feeding of females is proposed as a model for ape-hominid divergence through sexual selection; canine reduction is attributed to selection for associated epigamic displays. The analogy with male specialization through sexual selection speciation in hamadryas baboons is noted. Subsequent changes in female reproductive physiology are attributed to female competition for increased male parental investment during the time of early Homo andHomo erectus. The origin of higher intellectual and language abilities inHomo sapiens is attributed to male competition through technology and rule production to control resources and females; intellectual abilities involved in social manipulation are attributed to female competition for male parental investment and maintenance of polyandry. The course of hominid evolution is characterized as involving a trend from a promiscuous mating system toward increasing intensity of adaptations for male control of females, and by increasing intensity of female adaptation to maintain male parental investment while circumventing male control.     

Old males reduce melanin‐pigmented traits and increase reproductive outcome under worse environmental conditions in common kestrels

Secondary sexual traits displayed by males and females may have evolved as a signal of individual quality. However, both individual quality and investment on producing or maintaining enhanced sexual traits change as individuals age. At the same time, the costs associated to produce sexual traits might be attenuated or increased if environmental conditions are benign or worse respectively. Accordingly, environmental conditions are expected to shape the association between the expression of sexual traits and their reproductive outcome as individuals age. Nonetheless, little is known about the environmental influence on the co‐variation between sexual traits and reproductive outcome throughout the life of individuals. We studied the age‐dependency of the number and size of back spots, a melanin‐based and sexual trait in adults of common kestrels (Falco tinnunculus). We analysed the age‐dependence of reproductive traits and the environmental influence, defined as vole abundance, using a 10‐year individual‐based dataset. We broke down age‐related changes of reproductive traits into within‐ and between‐individual variation to assess their contribution to population‐level patterns. Our results showed a within‐individual decrease in the number, but not the size, of back spots in males. The size of back spots was positively correlated with food availability in males. Reproductive performance of males increased as they aged, in agreement with the life‐history theory but depending of vole abundance. Remarkably, we found that having fewer back spots was positively associated with clutch size only for old individuals under low‐food conditions. We suggest that environmental variation may shape the association between the expression of a sexual signal and reproductive outcome. We speculate that the reliability of sexual traits is higher when environmental conditions are poor only for old individuals. Within an evolutionary context, we suggest that the expression of sexual traits might be constrained by environmental conditions at later stages of life.     

Sister species diverge in modality‐specific courtship signal form and function

Understanding the relative importance of different sources of selection (e.g., the environment, social/sexual selection) on the divergence or convergence of reproductive communication can shed light on the origin, maintenance, or even disappearance of species boundaries. Using a multistep approach, we tested the hypothesis that two presumed sister species of wolf spider with overlapping ranges and microhabitat use, yet differing degrees of sexual dimorphism, have diverged in their reliance on modality‐specific courtship signaling. We predicted that male Schizocosa crassipalpata (no ornamentation) rely predominantly on diet‐dependent vibratory signaling for mating success. In contrast, we predicted that male S. bilineata (black foreleg brushes) rely on diet‐dependent visual signaling. We first tested and corroborated the sister‐species relationship between S. crassipalpata and S. bilineata using phylogenomic scale data. Next, we tested for species‐specific, diet‐dependent vibratory and visual signaling by manipulating subadult diet and subsequently quantifying adult morphology and mature male courtship signals. As predicted, vibratory signal form was diet‐dependent in S. crassipalpata, while visual ornamentation (brush area) was diet‐dependent in S. bilineata. We then compared the species‐specific reliance on vibratory and visual signaling by recording mating across artificially manipulated signaling environments (presence/absence of each modality in a 2 × 2 full factorial design). In accordance with our diet dependence results for S. crassipalpata, the presence of vibratory signaling was important for mating success. In contrast, the light and vibratory environment interacted to influence mating success in S. bilineata, with vibratory signaling being important only in the absence of light. We found no differences in overall activity patterns. Given that these species overlap in much of their range and microhabitat use, we suggest that competition for signaling space may have led to the divergence and differential use of sensory modalities between these sister species.     

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.     

Balancing sexual selection through opposing mate choice and male competition

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 reproductive and heterosexual behaviours of adult patas monkeys in captivity

The reproductive, agonistic, and social interactions between the adult male and adult females of a patas monkey (Erythrocebus patas) harem were investigated. The occurrence of oestrus appeared to be influenced by both social and hormonal factors. Oestrus was not limited to the peri-ovulatory period, but also occurred at other times within the menstrual cycle and after conception. Mating behaviour was correlated with seasonal decreases in daylength and temperature. The male showed no clear preference for either non-pregnant or pregnant sexual partners. Female dominance rank appeared to have little influence on intrasexual competition for copulations. Of the non-reproductive behaviours studied, only two (female-to-male grooming and heterosexual sitting-close) showed significant fluctuations in frequency with changing female reproductive state. For both behaviours, non-pregnant oestrous females showed the highest frequencies.