Does the potential strength of sexual selection differ between mating systems with and without defensive behaviours? A meta-analysis.

The Darwin-Bateman paradigm predicts that females enhance their fitness by being choosy and mating with high-quality males, while males should compete to mate with as many females as possible. In many species, males enhance their fitness by defending females and/or resources used by females. That is, males directly defend access to mating opportunities. However, paternity analyses have repeatedly shown that females in most species mate polyandrously, which contradicts traditional expectations that male defensive behaviours lead to monandry. Here, in an extensive meta-analysis, encompassing 109 species and 1026 effect sizes from across the animal kingdom, we tested if the occurrence of defensive behaviours modulates sexual selection on females and males. If so, we can illuminate the extent to which males really succeed in defending access to mating and fertilisation opportunities. We used four different indices of the opportunity for sexual selection that comprise pre-mating and/or post-mating episodes of selection. We found, for both sexes, that the occurrence of defensive behaviours does not modulate the potential strength of sexual selection. This implies that male defensive behaviours do not predict the true intensity of sexual selection. While the most extreme levels of sexual selection on males are in species with male defensive behaviours, which indicates that males do sometimes succeed in restricting females' re-mating ability (e.g. elephant seals, Mirounga leonina), estimates of the opportunity for sexual selection vary greatly across species, regardless of whether or not defensive behaviours occur. Indeed, widespread polyandry shows that females are usually not restricted by male defensive behaviours. In addition, our results indicate that post-mating episodes of selection, such as cryptic female choice and sperm competition, might be important factors modulating the opportunity for sexual selection. We discuss: (i) why male defensive behaviours fail to lower the opportunity for sexual selection among females or fail to elevate it for males; (ii) how post-mating events might influence sexual selection; and (iii) the role of females as active participants in sexual selection. We also highlight that inadequate data reporting in the literature prevented us from extracting effect sizes from many studies that had presumably collected the relevant data.

Male fattening is related to increased seminal quality of squirrel monkeys (Saimiri collinsi): Implications for sperm competition.

Saimiri are neotropical primates with seasonal reproduction, males develop a seasonal fattening condition that has been suggested as a pre-copulatory sexual selection strategy. Furthermore, females mate with multiple males in the same season. This could also favor the evolution of a postcopulatory sexual strategy by sperm competition. In this study, we tested the hypothesis that there is a relationship between the fatted condition and advantageous seminal characteristics in Saimiri collinsi and evaluated its implications for sperm competition. Adult males (N = 10), aged 5-15 years, housed in mixed or only-male groups, were analyzed from June, 2015 to July, 2016. Measurements of weight, axilla, and arm skinfold, and testicular volume were taken monthly, and semen was collected by electroejaculation. A fattening index was developed to quantify and identify fatted males, biometrics, and seminal parameters were compared between the non-fatted and fatted conditions. The fatted males present a larger testicular volume. This is related to the increase in spermatogenic activity necessary to sustain a high ejaculation frequency during the mating season. An increase in seminal volume and in frequency of semen coagulation were detected in fatted males, advantages related to sperm protection in the female reproductive tract. Age and social context were not significant sources of variation for both morphological and seminal traits. A decrease in response from the fatted males in obtaining semen and an increase in the frequency of azoospermic ejaculates were observed. These unexpected results may be due to intense reproductive activities in a short period. The fattening phenomenon has many implications in the sexual selection of squirrel monkeys, and they are still not entirely unveiled. Our results corroborate the idea that, in S. collinsi, the fatted male condition is related to sexual selection, and we found evidence suggesting it may be also expressed by a post-copulatory component, sperm competition.

Male Age Influences Re-mating Incidence and Sperm Use in Females of the Dengue Vector Aedes aegypti.

Diseases transmitted by female Aedes aegypti mosquitoes are public health issues in countries in the tropics and sub-tropics. As in other insects, A. aegypti females undergo behavioral and physiological changes upon mating that principally act to facilitate the production of progeny. The primary effectors of A. aegypti female post-mating responses are male-derived seminal proteins that are transferred to females during mating. Increased male age reduces ejaculate function in numerous taxa and alters seminal protein composition in Drosophila melanogaster, but the impacts of male age on female A. aegypti post-mating responses are unknown. Here, we used "old" (21-22 days old) and "young" (4-5 days old) A. aegypti males to assess the influence of male age on oviposition, fertility, and re-mating incidence in their mates. We also examined how age influenced paternity share in females initially mated to young or old males that subsequently re-mated with a transgenic male that transferred RFP-labeled sperm and whose progeny inherited a larval-expressed GFP marker. We found that increased male age had no effect on female fecundity or fertility but significantly impacted their ability to prevent re-mating in their mates-more than half (54.5%) of the females mated to an old male re-mated, compared to 24% of females initially mated to a young male. Polyandrous A. aegypti females displayed first male precedence regardless of the age of their initial mate. However, young males were better able to compete with rival male sperm, siring significantly more progeny (77%) compared to old males (64%). Young males had significantly more sperm in their seminal vesicles than old males at the time of mating, although males of both age groups transferred similar numbers of sperm to their mates. Our results suggest that male senescence differentially impacts the induction of some post-mating changes in A. aegypti females. As the effect of age may be further exacerbated in the field, age-related declines in male ability to induce sexual refractoriness have implications for A. aegypti population control programs that release adults into the environment.

Functional morphology of the sperm-containing chambers of the sea slug Okenia polycerelloides in the context of sexual selection.

Sea slugs are interesting models to study post-copulatory sexual selection in simultaneous hermaphrodites due to the enormous variation of their reproductive systems. However, the knowledge of the functional morphology of their reproductive system is limited to few species, and it is rarely discussed in the context of sexual selection theory. In this study, we investigated the functional morphology of the sperm-containing chambers (i.e., ampulla, seminal receptacle, and bursa copulatrix) of the reproductive system of Okenia polycerelloides (Ortea & Bouchet, 1983), based on light, confocal, and electron microscopy. Although the morphology of the ampulla is similar to other species, indicating that it is a site for autosperm storage, we found some sperm facing the ampullar epithelium, a feature commonly regarded as characteristic of the seminal receptacle of sea slugs. The seminal receptacle of O. polycerelloides showed secretory activity and contained sperm with distribution and orientation suggestive of stratification of allosperm from distinct mating events, a feature that would affect sperm competition. The bursa copulatrix had epithelial cells with secretory and absorptive characteristics, and contained degraded sperm and yolk granules within its lumen. Comparative analyses of the contents of each organ demonstrated that sperm digestion occurs in the bursa copulatrix and affects sperm heads first, changing their morphology from slender and curved to shorter and ellipsoid before complete lysis. Although digestion and absorption of surplus sperm are currently the main hypothesized functions for the bursa copulatrix, its role in cryptic female choice should not be ruled out. The close structural connection between the seminal receptacle and bursa copulatrix, as well as their muscular walls, would enable control over the fate of the sperm received in each mating event, that is, storage or digestion.

Female sperm storage mediates post-copulatory costs and benefits of ejaculate anticipatory plasticity in the guppy.

Males of many species evolved the capability of adjusting their ejaculate phenotype in response to social cues to match the expected mating conditions. When females store sperm for a prolonged time, the expected fitness return of plastic adjustments of ejaculate phenotype may depend on the interval between mating and fertilization. Although prolonged female sperm storage (FSS) increases the opportunity for sperm competition, as a consequence of the longer temporal overlap of ejaculates from several males, it may also create variable selective forces on ejaculate phenotype, for example by exposing trade-offs between sperm velocity and sperm survival. We evaluated the relationship between the plasticity of ejaculate quality and FSS in the guppy, Poecilia reticulata, a polyandrous live-bearing fish in which females store sperm for several months and where stored sperm contribute significantly to a male's lifelong reproductive success. In this species, males respond to the perception of future mating opportunities by increasing the quantity (number) and quality (swimming velocity) of ready-to-use sperm (an anticipatory response called 'sperm priming'). Here we investigated (a) the effect of sperm priming on in vitro sperm viability at stripping and its temporal decline (as an estimate of sperm survival), and (b) the in vivo competitive fertilization success in relation to female sperm storage using artificial insemination. As expected, sperm-primed males produced more numerous and faster sperm, but with a reduced in vitro sperm viability at stripping and after 4 hr, compared with their counterparts. Artificial insemination revealed that the small (nonsignificant) advantage of primed sperm when fertilization immediately follows insemination is reversed when eggs are fertilized by female-stored sperm, weeks after insemination. By suggesting a plastic trade-off between sperm velocity and viability, these results demonstrate that prolonged female sperm storage generates divergent selection pressures on ejaculate phenotype.

Sexual Selection and the Evolution of Male Reproductive Traits in Benthic Octopuses.

Competition between same-sex organisms, or intra-sexual selection, can occur before and after mating, and include processes such as sperm competition and cryptic female choice. One of the consequences of intra-sexual selection is that male reproductive traits tend to evolve and diverge at high rates. In benthic octopuses, females often mate with more than one male in a single reproductive event, opening the venue for intra-sexual selection at multiple levels. For instance, males transfer spermatophores through hectocotylus, and can remove the spermatophores left by other males. Considering the limited evidence on post-copula competition in benthic octopuses, and the potential to affect the evolution of reproductive traits within octopodids, we put this hypothesis to a test employing a phylogenetic comparative approach. We combined data on hectocotylized arm length (HAL), ligula length (LL), spermatophore length (SL) with a Bayesian molecular phylogeny of 87 species, to analyze how reproductive traits have diverged across lineages and covary with body size (mantle length; ML). First, additionally to ML, we estimated the phylogenetic signal (λ) and mode of evolution (κ) in each reproductive trait. Second, we performed phylogenetic regressions to quantify the association among reproductive traits and their co-variation with ML. This analysis allowed us to estimate the phenotypic change along a branch into the phylogeny, and whether selection may have played a role in the evolution and diversification of specific clades. Estimations of λ were always high (>0.75), indicating concordance between the traits and the topology of the phylogenetic tree. Low values of κ (<1.0) suggested that evolution depends on branch lengths. All reproductive traits exhibiting a positive relation with ML (ß > 0.5 in all cases). Overall, evolutionary rate models applied to the SL-ML regression suggested that octopuses of the family Megaleledonidae have evolved larger spermatophores than expected for their size. The regression HAL-ML indicated that HAL was more variable in Megaleledonidae than in the remaining clades, suggesting that the high divergence across species within this group might partially reflect intra-sexual selection. These results support the hypothesis that, at least in some lineages, sexual selection may account for the divergence in reproductive traits of male octopuses.

Sperm Morphology in Neotropical Primates.

The morphological and morphometric characterization of spermatozoa has been used as a taxonomic and phylogenetic tool for different species of mammals. We evaluated and compared the sperm morphometry of five neotropical primate species: Alouatta caraya, Ateles belzebuth and Ateles chamek of family Atelidae; and Cebus cay (=Sapajus cay) and Cebus nigritus (=Sapajus nigritus) of family Cebidae. After the collection of semen samples, the following parameters were measured on 100 spermatozoa from each specimen: Head Length, Head Width, Acrosome Length, Midpiece Length, Midpiece Width and Tail Length. Considering the available literature on sperm morphometry, we gathered data of 75 individuals, from 20 species, 8 genera and 2 families. These data were superimposed on a phylogeny to infer the possible direction of evolutionary changes. Narrower and shorter spermatozoa seem to be the ancestral form for Cebidae, with a trend toward wider and larger heads in derived groups. The spermatozoa of Atelidae may show an increase in total length and midpiece length. Sperm heads would have become narrower in the more derived groups of Ateles. Sperm length may increase in the more derived species in both families. Our results are discussed in the context of sperm competition and sexual selection.

Individual asymmetry as a predictor of fitness in the bat Carollia perspicillata.

The measurement of fitness in wild populations is a challenging task, and a number of proxies have been proposed with different degrees of success. Developmental instability/stability (DI) is an organismal property associated with variance in bilateral asymmetry (fluctuating asymmetry-FA) and a correlated effect on fitness. This study provides evidence to corroborate the hypothesis that asymmetry partly reflects DI and is correlated with a reduction in fitness measured by survival and reproduction in bats. We studied two colonies of the bat Carollia perspicillata in southeastern Brazil over 5 years, marking and recapturing individuals. Gaussian mixture models for signed Forearm Asymmetry (ForA) distribution indicated that ~20% of asymmetry variation was due to DI heterogeneity among individuals. ForA, body condition (Scaled Mass Index-SMI) and Forearm Length (ForL) were used as predictors of survival probability in Cormack-Jolly-Seber models. Asymmetry was negatively associated with survival, whereas SMI and ForL were positively associated. The male C. perspicillata defend sites within the roost that are favoured by female harems, but there are mating opportunities for bachelor males, leading to both territorial disputes and sperm competition. As predicted by sexual selection, ForA was negatively associated with relative Testicle Length, a measure of reproductive potential. In females, ForA was negatively associated with the probability of two pregnancies (as opposed to one) in a given breeding season. The effect magnitudes and directions of associations suggest that asymmetry, even though not perfectly reflecting DI variation, is a useful predictor for fitness components in C. perspicillata.

Possible glimpses into early speciation: the effect of ovarian fluid on sperm velocity accords with post-copulatory isolation between two guppy populations.

Identifying mechanisms of reproductive isolation is key to understanding speciation. Among the putative mechanisms underlying reproductive isolation, sperm-female interactions (post-mating-prezygotic barriers) are arguably the hardest to identify, not least because these are likely to operate at the cellular or molecular level. Yet sperm-female interactions offer great potential to prevent the transfer of genetic information between different populations at the initial stages of speciation. Here, we provide a preliminary test for the presence of a putative post-mating-prezygotic barrier operating between three populations of Trinidadian guppies (Poecilia reticulata), an internally fertilizing fish that inhabits streams with different levels of connectivity across Trinidad. We experimentally evaluate the effect of female ovarian fluid on sperm velocity (a predictor of competitive fertilization success) according to whether males and females were from the same (native) or different (foreign) populations. Our results reveal the potential for ovarian fluid to act as a post-mating-prezygotic barrier between two populations from different drainages, but also that the strength of this barrier is different among populations. This result may explain the previous finding that, in some populations, sperm from native males have precedence over foreign sperm, which could eventually lead to reproductive isolation between these populations.

Redescription and first record in South America of Neogriphoneura timida Curran (Diptera, Lauxaniidae)

ABSTRACT The genus Neogriphoneura Malloch, 1924 is currently composed of 11 species with New World distribution. Neogriphoneura timida Curran, 1942 is recorded for the first time in South America, with occurrences in Brazil, Colombia and Trinidad and Tobago; and new Central American records are presented: Belize, Honduras and Mexico. Here we redescribe the species and present, for the first time, illustrations of the male terminalia and female spermathecae, and discuss the main diagnostic characteristics of external morphology. A brief discussion about the postcopulatory sexual selection in this species is proposed based on morphology of the spermathecae.

Rapid differentiation and asynchronous coevolution of male and female genitalia in stink bugs.

Despite claims that genitalia are among the fastest evolving phenotypes, few studies have tested this trend in a quantitative and phylogenetic framework. In systems where male and female genitalia coevolve, there is a growing effort to explore qualitative patterns of evolution and their underlying mechanisms, but the temporal aspect remains overlooked. An intriguing question is how fast male and female genitalia may change in a coevolutionary scenario. Here, we apply a series of comparative phylogenetic analyses to reveal a scenario of correlated evolution and to investigate how fast male and female external, nonhomologous and functionally integrated genitalia change in a group of stink bugs. We report three findings: the female gonocoxite 8 and the male pygophore showed a clear pattern of correlated evolution, both genitalia were estimated to evolve much faster than nongenital traits, and rates of evolution of the male genitalia were twice as fast as the female genitalia. Our results corroborate the widely held view that male genitalia evolve fast and add to the scarce evidence for rapidly evolving female genitalia. Different rates of evolution exhibited by males and females suggest either distinct forms or strengths of selection, despite their tight functional integration and coevolution. The morphological characteristics of this coevolutionary trend are more consistent with a cooperative adjustment of the genitalia, suggesting a scenario of female choice, morphological accommodation, lock-and-key or some combination of the three.

Is Juvenile Hormone a potential mechanism that underlay the "branched Y-model"?

Trade-offs are a central tenet in the life-history evolution and the simplest model to understand it is the "Y" model: the investment of one arm will affect the investment of the other arm. However, this model is by far more complex, and a "branched Y-model" is proposed: trade-offs could exist within each arm of the Y, but the mechanistic link is unknown. Here we used Tenebrio molitor to test if Juvenile Hormone (JH) could be a mechanistic link behind the "branched Y-model". Larvae were assigned to one of the following experimental groups: (1) low, (2) medium and (3) high doses of methoprene (a Juvenile Hormone analogue, JHa), (4) acetone (methoprene diluents; control one) or (5) näive (handled in the same way as other groups; control two). The JHa lengthened the time of development from larvae to pupae and larvae to adults, resulting in adults with a larger size. Males with medium and long JHa treatment doses were favored with female choice, but had smaller testes and fewer viable sperm. There were no differences between groups in regard to the number of spermatozoa of males, or the number of ovarioles or eggs of females. This results suggest that JH: (i) is a mechanistic link of insects "branched Y model", (ii) is a double ended-sword because it may not only provide benefits on reproduction but could also impose costs, and (iii) has a differential effect on each sex, being males more affected than females.

Male facial attractiveness and masculinity may provide sex- and culture-independent cues to semen quality.

Phenotype-linked fertility hypothesis (PLFH) predicts that male secondary sexual traits reveal honest information about male fertilization ability. However, PLFH has rarely been studied in humans. The aim of the present study was to test PLFH in humans and to investigate whether potential ability to select fertile partners is independent of sex or cultural background. We found that on the contrary to the hypothesis, facial masculinity was negatively associated with semen quality. As increased levels of testosterone have been demonstrated to impair sperm production, this finding may indicate a trade-off between investments in secondary sexual signalling (i.e. facial masculinity) and fertility or status-dependent differences in investments in semen quality. In both sexes and nationalities (Spanish and Colombian), ranked male facial attractiveness predicted male semen quality. However, Spanish males and females estimated facial images generally more attractive (gave higher ranks) than Colombian raters, and in both nationalities, males gave higher ranks than females. This suggests that male facial cues may provide culture- and sex-independent information about male fertility. However, our results also indicate that humans may be more sensitive to facial attractiveness cues within their own populations and also that males may generally overestimate the attractiveness of other men to females.

Multiple paternity and sperm competition in the sibling species Drosophila buzzatii and Drosophila koepferae.

Sperm competition (SC) is a major component of sexual selection that enhances intra- and intersexual conflicts and may trigger rapid adaptive evolution of sexual characters. The actual role of SC on rapid evolution, however, is poorly understood. Besides, the relative contribution of distinctive features of the mating system to among species variation in the strength of SC remains unclear. Here, we assessed the strength of SC and mating system factors that may account for it in the closely related species Drosophila buzzatii and Drosophila koepferae. Our analyses reveal higher incidence of multiple paternity and SC risk in D. buzzatii wild-inseminated females. The estimated number of fathers per brood was 3.57 in D. buzzatii and 1.95 in D. koepferae. In turn, the expected proportion of females inseminated by more than one male was 0.89 in D. buzzatii and 0.58 in D. koepferae. Laboratory experiments show that this pattern may be accounted for by the faster rate of stored sperm usage observed in D. koepferae and by the greater female remating rate exhibited by D. buzzatii. We also found that the male reproductive cost of SC is also higher in D. buzzatii. After a female mated with a second male, first-mating male fertility was reduced by 71.4% in D. buzzatii and only 33.3% in D. koepferae. Therefore, we may conclude that postmating sexual selection via SC is a stronger evolutionary force in D. buzzatii than in its sibling.

Does Patriline Composition Change over a Honey Bee Queen's Lifetime?

A honey bee queen mates with a number of drones a few days after she emerges as an adult. Spermatozoa of different drones are stored in her spermatheca and used for the rest of the queen's life to fertilize eggs. Sperm usage is thought to be random, so that the patriline distribution within a honey bee colony would remain constant over time. In this study we assigned the progeny of a naturally mated honey bee queen to patrilines using microsatellite markers at the queen's age of two, three and four years. No significant changes in patriline distribution occurred within each of two foraging seasons, with samples taken one and five months apart, respectively. Overall and pair-wise comparisons between the three analyzed years reached significant levels. Over the three-year period we found a trend for patrilines to become more equally represented with time. It is important to note that this study was performed with a single queen, and thus individual and population variation in sperm usage patterns must be assessed. We discuss long-term changes in patriline composition due to mixing processes in the queen's spermatheca, following incomplete mixing of different drones' sperm after mating.

Testis size, epididymis weight, and sperm competition in rhesus macaques.

The intensity of sperm competition is often measured using the gonadosomatic index (testes/body weight). But sperm competition could be mediated more by size of the epididymis than by size of the testicles, and little information is available on the relationship between testicular and epididymal size. We found that both organs were positively correlated in size among male rhesus macaques. Body weight accounted for over 70% of the variance in testicle size and volumetric estimates of testicle size accurately reflected testicle weight. We conclude that methods for ascertaining testicle size are accurate, but the covariation in size between testicles and epididymis will hamper understanding of the physiological mechanisms involved in sperm competition in primates. © 1993 Wiley-Liss, Inc.