Mechanisms Of Sexual Selection Research Articles

The surprising complexity and diversity of sperm storage structures across Galliformes.

In internal fertilisers, the precise timing of ovulation with the arrival of sperm at the site of fertilisation is essential for fertilisation success. In birds, mating is often not synchronised with ovulation, but instead females utilise specialised sperm storage tubules (SSTs) in the reproductive tract, which can ensure sperm are always available for fertilisation at the time of ovulation, whilst simultaneously providing a mechanism of post-copulatory sexual selection. Despite the clear importance of SSTs for fertilisation success, we know little about the mechanisms involved in sperm acceptance, storage, and release. Furthermore, most research has been conducted on only a small number of species, based on which SSTs are usually assumed to look and function in the same way across all species. Here, we conduct a comparative exploration of SST morphology across 26 species of Galliformes. We show that SSTs, and the surrounding tissue, can vary significantly in morphology across species. We provide observational evidence that Galliformes exhibit at least 5 distinct categories of tubule types, including distinctive coiled and multi-branched tubules, and describe 2 additional features of the surrounding tissue. We suggest functional explanations for variation in tubule morphology and propose next steps for future research. Our findings indicate that SSTs are likely to be far more variable than has previously been assumed, with potentially important consequences for our understanding of sperm storage in birds and post-copulatory sexual selection in general.

Sperm competition favours intermediate sperm size in a hermaphrodite1.

Sperm competition is a potent mechanism of postcopulatory sexual selection that has been found to shape reproductive morphologies and behaviours in promiscuous animals. Especially sperm size has been argued to evolve in response to sperm competition through its effect on sperm longevity, sperm motility, the ability to displace competing sperm, and ultimately fertilization success. Additionally, sperm size has been observed to co-evolve with female reproductive morphology. Theoretical work predicts that sperm competition may select for longer sperm but may also favour shorter sperm if sperm size trades-off with number. In this study, we studied the relationship between sperm size and postmating success in the free-living flatworm, Macrostomum lignano. Specifically, we used inbred isolines of M. lignano that varied in sperm size to investigate how sperm size translated into the ability of worms to transfer and deposit sperm in a mating partner. Our results revealed a hump-shaped relationship with individuals producing sperm of intermediate size having the highest sperm competitiveness. This finding broadens our understanding of the evolution of sperm morphology by providing empirical support for stabilizing selection on sperm size under sperm competition.

Paternity bias and cryptic female choice in chickens

Sperm competition and cryptic female choice (CFC) are two significant mechanisms of postcopulatory sexual selection that greatly impact fertilization success in various species. Despite extensive research has conducted on sperm competition and the evolution of sperm traits in internal fertilizers, our understanding of the female preferences in selecting sperm is still limited. Here, we aimed to investigate the characteristics of CFC in chickens by utilizing artificial insemination with mixed semen to control for variations in male fertilization success caused by female perception of male quality and mating order. Our results revealed that the offspring from multiple-mated females exhibited mixed paternity. Although the males had an equal number of viable sperm, one male consistently exhibited a 15% higher success rate on average, regardless of whether the insemination was performed with fresh or diluted semen. This result suggested that this male demonstrates superior performance in sperm competition, and exhibited a potential advantage in fertilization success. While the dominant male generally made a greater genetic contribution to most offspring, the degree of this advantage varied greatly, ranging from 11.11% to 75.00%. Furthermore, our study provided evidence of female preferences influenced the precedence of sperm from certain males over others. Interestingly, this bias is not consistently observed among all individuals, as offspring derived from some females were predominantly sired by an overall disadvantaged male while others were predominantly by a different disadvantaged male. Overall, these results underscored the complex processes involved in sperm selection and emphasized the importance of females in sexual selection theory.

Inferred Attractiveness: A generalized mechanism for sexual selection that can maintain variation in traits and preferences over time.

Sexual selection by mate choice is a powerful force that can lead to evolutionary change, and models of why females choose particular mates are central to understanding its effects. Predominant mate choice theories assume preferences are determined solely by genetic inheritance, an assumption still lacking widespread support. Moreover, preferences often vary among individuals or populations, fail to correspond with conspicuous male traits, or change with context, patterns not predicted by dominant models. Here, we propose a new model that explains this mate choice complexity with one general hypothesized mechanism, "Inferred Attractiveness." In this model, females acquire mating preferences by observing others' choices and use context-dependent information to infer which traits are attractive. They learn to prefer the feature of a chosen male that most distinguishes him from other available males. Over generations, this process produces repeated population-level switches in preference and maintains male trait variation. When viability selection is strong, Inferred Attractiveness produces population-wide adaptive preferences superficially resembling "good genes." However, it results in widespread preference variation or nonadaptive preferences under other predictable circumstances. By casting the female brain as the central selective agent, Inferred Attractiveness captures novel and dynamic aspects of sexual selection and reconciles inconsistencies between mate choice theory and observed behavior.

Geometric morphometric analysis of the variations in cephalothorax shape of the freshwater prawn Macrobrachium tenellum, Smith (Decapoda Palaemonidae) from two different coastal basins in Oaxaca, Mexico

Morphological variations of Macrobrachium tenellum prawns from two populations from locations in the Copalita and Colotepec riverine basins in the seashore of Oaxaca, Mexico, were studied with geometric morphometry techniques. The purpose was to find and explain significant differences in shape and size between the cephalothorax and the rostrum. Differences between sexes and populations were intended to prove intra and inter-populations. Results suggest low intrapopulation differences but significant interpopulation variation between specimens from different places, while a regression analysis suggests a higher correlation between shape and size only in males. The higher differences in places between and within sexes could be explained due to differences in environmental pressure. A positive allometry bias in males could indicate a sexual selection mechanism affecting mating.

Sexual dimorphism in the lacertid lizard Apathya cappadocica (Werner, 1902) (Reptilia: Lacertidae) from southeastern Türkiye

Apathya cappadocica is a medium-sized lizard species included in the family Lacertidae. The species is known from Türkiye, Northern Syria, Iraq, and Western Iran. Sexual dimorphism (SD), which is a phenomenon including phenotypic differences between males and females, has many effects on behaviour, shape and size characteristics. A total of 87 adult lizard specimens collected from south-eastern Anatolia were used in this study. The results of ANOVA showed that all morphometric features exhibited a pattern in which males have larger size than females. According to principal component analysis (PCA), the first three factors explain 81.553% of the total variance. Differences in head size between sexes have been well-documented in lizards and are associated with male-male aggression which results in mating success. This kind of pattern is supported by this study. Additionally, the results showed that males have more femoral pores, which is a signalling mechanism for sexual selection, than females. In conclusion, it can be accepted that the species in the genus Apathya has a similar pattern in accordance with the larger male theory.

Drivers and consequences of female reproductive competition in an egalitarian, sexually monomorphic primate

Even after the 150th anniversary of sexual selection theory, the drivers and mechanisms of female sexual selection remain poorly studied. To understand demographic circumstances favoring female-female competition, trade-offs with kin selection and interactions with male reproductive strategies, we investigated female evictions in redfronted lemurs (Eulemur rufifrons). Based on 24 years of demographic data of known individuals, we show that female redfronted lemurs target close female kin for forcible, permanent, and presumably lethal eviction, even though groups contain multiple unrelated males whose voluntary emigration actually mitigated the probability of future female evictions. Female eviction and male emigration were predicted by group size, but male emigration was primarily driven by a proportional increase of male rivals. Female evictions were more likely than male emigrations when there were more juvenile females in a group, but the identity of evicted females was not predicted by any intrinsic traits. While birth rates were reduced by the number of juvenile females, they were higher when there were more adult females in a group and in years with more rainfall. Early infant survival was reduced with increasing numbers of juvenile females, but variation in female lifetime reproductive success was not related to any of the predictors examined here. Thus, there seems to be a limit on female group size in this lemur species. More generally, our study demonstrates a balanced interplay between female reproductive competition, competition over group membership between both sexes, and kin selection, contributing new insights into the causes and consequences of female competition in animal societies.Significance statementThe evolutionary causes of female competition in vertebrate societies remain poorly known. Evictions represent an extreme form of female competition because even close kin are evicted when same-sized unrelated males are theoretically also available as victims. We studied drivers and consequences of evictions in redfronted lemurs (Eulemur rufifrons) using 24 years of demographic data from multiple groups. We show that while voluntary male emigration mitigates the probability of future female evictions, females nonetheless appear to accept the fitness costs of evicting female kin. While group size seems to be the main driver of departures by either sex, the number of juvenile females present in groups is the key variable triggering eviction events as well as physiological responses that could be interpreted as female reproductive restraint. Our study therefore revealed that competition does trump cooperation under some circumstances in the intricate interplay between sexual selection and kin selection on females.

Baculum shape complexity correlates to metrics of post-copulatory sexual selection in Musteloidea.

The penis bone, or baculum, is present in many orders of mammals, although its function is still relatively unknown, mainly due to the challenges with studying the baculum in vivo. Suggested functions include increasing vaginal friction, prolonging intromissionand inducing ovulation. Since it is difficult to study baculum function directly, functional morphology can give important insights. Shape complexity techniques, in particular, are likely to offer a useful metric of baculum morphology, especially since finding homologous landmarks on such a structure is challenging. This study focuses on measuring baculum shape complexity in the Musteloidea-a large superfamily spanning a range of body sizes with well-developed, qualitatively diverse bacula. We compared two shape complexity metrics-alpha shapes and ariaDNE and conducted analyses over a range of six different coefficients, or bandwidths, in 32 species of Musteloidea. Overall, we found that shape complexity, especially at the baculum distal tip, is associated with intromission duration using both metrics. These complexities can include hooks, bifurcationsand other additional projections. In addition, alpha shapes complexity was also associated with relative testes mass. These results suggest that post-copulatory mechanisms of sexual selection are probably driving the evolution of more complex-shaped bacula tips in Musteloidea and are likely to be especially involved in increasing intromission duration during copulation.

Evolution of sexually selected traits across animals

Sexual selection is thought to be a major driver of phenotypic diversity and diversification in animals, but large-scale evolutionary patterns in sexually selected (SS) traits remain largely unknown. Here, we survey and analyze the evolution of these traits across animal phylogeny. We find that female mate choice appears to be the most widespread mechanism of sexual selection, but male-male competition appears to be almost as frequent in chordates and male mate choice is also common in arthropods. Among sensory types, tactile traits appear to be most widespread whereas auditory traits are relatively uncommon. Rather than being ubiquitous or randomly distributed across animals, most of these different types of SS traits are confined to clades in arthropods and chordates, which form “hotspots” for the evolution of these diverse trait types. Thus, different sensory types show accelerated rates of evolution in these clades. Moreover, different types of SS traits are strongly correlated with each other in their evolution across animals. Finally, despite the intensive interest in the role of sexual selection in speciation, we find only limited support for the idea that SS traits drive large-scale patterns of diversification and species richness across all animals.

Sexual Selection in Insects

Sexual selection is an evolutionary process, that increases the direct and indirect fitness of an organism by non random preference of mates, based on their differential ability. Sexual selection may be in the form of intrasexual selection and intersexual selection. The former involves competition between the males (usually), while females are passive acceptors of winners as mates. The latter involves display of abilities by the males (usually), while the female inspects and assesses them prior to selection of mate. Traditionally both these mechanisms are believed to take place prior to copulation. However, studies indicate that these also take place, post copulation. The post copulatory displays of sexual selection involve sperm competition and cryptic female choice. Not only are all these displays fascinating, understanding their evolution and their ecological modulations make this field an interesting one. This review deals with these aspects of sexual selection in insects, as they encase some of the most diverse mechanisms of sexual selection.

Haemosporidian parasites and incubation period influence plumage coloration in tanagers (Passeriformes: Thraupidae).

Birds are highly visually oriented and use plumage coloration as an important signalling trait in social communication. Hence, males and females may have different patterns of plumage coloration, a phenomenon known as sexual dichromatism. Because males tend to have more complex plumages, sexual dichromatism is usually attributed to female choice. However, plumage coloration is partly condition-dependent; therefore, other selective pressures affecting individuals' success may also drive the evolution of this trait. Here, we used tanagers as model organisms to study the relationships between dichromatism and plumage coloration complexity in tanagers with parasitism by haemosporidians, investment in reproduction and life-history traits. We screened blood samples from 2849 individual birds belonging to 52 tanager species to detect haemosporidian parasites. We used publicly available data for plumage coloration, bird phylogeny and life-history traits to run phylogenetic generalized least-square models of plumage dichromatism and complexity in male and female tanagers. We found that plumage dichromatism was more pronounced in bird species with a higher prevalence of haemosporidian parasites. Lastly, high plumage coloration complexity in female tanagers was associated with a longer incubation period. Our results indicate an association between haemosporidian parasites and plumage coloration suggesting that parasites impact mechanisms of sexual selection, increasing differences between the sexes, and social (non-sexual) selection, driving females to develop more complex coloration.

The evolutionary history and spectral tuning of vertebrate visual opsins

Many animals depend on the sense of vision for survival. In eumetazoans, vision requires specialized, light-sensitive cells called photoreceptors. Light reaches the photoreceptors and triggers the excitation of light-detecting proteins called opsins. Here, we describe the story of visual opsin evolution from the ancestral bilaterian to the extant vertebrate lineages. We explain the mechanisms determining color vision of extant vertebrates, focusing on opsin gene losses, duplications, and the expression regulation of vertebrate opsins. We describe the sequence variation both within and between species that has tweaked the sensitivities of opsin proteins towards different wavelengths of light. We provide an extensive resource of wavelength sensitivities and mutations that have diverged light sensitivity in many vertebrate species and predict how these mutations were accumulated in each lineage based on parsimony. We suggest possible natural and sexual selection mechanisms underlying these spectral differences. Understanding how molecular changes allow for functional adaptation of animals to different environments is a major goal in the field, and therefore identifying mutations affecting vision and their relationship to photic selection pressures is imperative. The goal of this review is to provide a comprehensive overview of our current understanding of opsin evolution in vertebrates.

MAIA, Fc receptor-like 3, supersedes JUNO as IZUMO1 receptor during human fertilization.

Gamete fusion is a critical event of mammalian fertilization. A random one-bead one-compound combinatorial peptide library represented synthetic human egg mimics and identified a previously unidentified ligand as Fc receptor–like 3, named MAIA after the mythological goddess intertwined with JUNO. This immunoglobulin super family receptor was expressed on human oolemma and played a major role during sperm-egg adhesion and fusion. MAIA forms a highly stable interaction with the known IZUMO1/JUNO sperm-egg complex, permitting specific gamete fusion. The complexity of the MAIA isotype may offer a cryptic sexual selection mechanism to avoid genetic incompatibility and achieve favorable fitness outcomes.

Vocal Cues to Male Physical Formidability.

Animal vocalizations convey important information about the emitter, including sex, age, biological quality, and emotional state. Early on, Darwin proposed that sex differences in auditory signals and vocalizations were driven by sexual selection mechanisms. In humans, studies on the association between male voice attributes and physical formidability have thus far reported mixed results. Hence, with a view to furthering our understanding of the role of human voice in advertising physical formidability, we sought to identify acoustic attributes of male voices associated with physical formidability proxies. Mean fundamental frequency (F0), formant dispersion (Df), formant position (Pf), and vocal tract length (VTL) data from a sample of 101 male voices was analyzed for potential associations with height, weight, and maximal handgrip strength (HGS). F0 correlated negatively with HGS; Pf showed negative correlations with HGS, height and weight, whereas VTL positively correlated with HGS, height and weight. All zero-order correlations remained significant after controlling for false discovery rate (FDR) with the Benjamini–Hochberg method. After controlling for height and weight—and controlling for FDR—the correlation between F0 and HGS remained significant. In addition, to evaluate the ability of human male voices to advertise physical formidability to potential mates, 151 heterosexual female participants rated the voices of the 10 strongest and the 10 weakest males from the original sample for perceived physical strength, and given that physical strength is a desirable attribute in male partners, perceived attractiveness. Generalized linear mixed model analyses—which allow for generalization of inferences to other samples of both raters and targets—failed to support a significant association of perceived strength or attractiveness from voices alone and actual physical strength. These results add to the growing body of work on the role of human voices in conveying relevant biological information.

Endurance rivalry and female choice jointly influence male mating success in the emerald treefrog (Zhangixalus prasinatus), a lek-chorusing anuran

BackgroundEndurance rivalry and female choice are two important mechanisms of sexual selection in lek-breeding species. Endurance rivalry is when males compete for opportunities to mate by spending more time in leks than others (interaction-independent male-male competition). Because high-quality males can afford to have high lek attendance, females have a higher chance of mating with good-quality males even when they mate randomly. The good gene hypothesis proposes that females can pass good genes on to their offspring by choosing males that display elaborate morphological and/or behavioral traits that reflect the males’ genetic quality. The relative importance of lek attendance and female choice to males’ mating success in anurans is rarely evaluated. In this study, we investigated how these two mechanisms might jointly shape males’ morphological traits in the lek-chorusing emerald treefrog Zhangixalus prasinatus.ResultsOur results show that (1) male lek attendance is positively correlated with body size and condition, and males with higher lek attendance have higher mating success, (2) the dominant frequency of males’ advertisement calls are negatively correlated with body size and males producing lower frequency calls have higher mating success, (3) male body size, but not body condition, has a non-significant positive relationship with mating success and (4) females show preference for calls with lower dominant frequencies in two-choice playback.ConclusionsOverall, both endurance rivalry and female choice play an important role in the mating success of male emerald treefrogs in the field and both are influenced by male body size/condition. By mating with males that have higher lek attendance and produce lower frequency calls, selection may indirectly favor larger males.

Drosophila female reproductive glands contribute to mating plug composition and the timing of sperm ejection.

Reproductive traits that influence female remating and competitive fertilization rapidly evolve in response to sexual selection and sexual conflict. One such trait, observed across diverse animal taxa, is the formation of a structural plug inside the female reproductive tract (FRT), either during or shortly after mating. In Drosophila melanogaster, male seminal fluid forms a mating plug inside the female bursa, which has been demonstrated to influence sperm entry into storage and latency of female remating. Processing of the plug, including its eventual ejection from the female's reproductive tract, influences the competitive fertilization success of her mates and is mediated by female × male genotypic interactions. However, female contributions to plug formation and processing have received limited attention. Using developmental mutants that lack glandular FRT tissues, we reveal that these tissues are essential for mating plug ejection. We further use proteomics to demonstrate that female glandular proteins, and especially proteolytic enzymes, contribute to mating plug composition and have a widespread impact on plug formation and composition. Together, these phenotypic and molecular data identify female contributions to intersexual interactions that are a potential mechanism of post-copulatory sexual selection.

The ontogeny of sexual dimorphism in free-ranging rhesus macaques.

Reconstructing the social lives of extinct primates is possible only through an understanding of the interplay between morphology, sexual selection pressures, and social behavior in extant species. Somatic sexual dimorphism is an important variable in primate evolution, in part because of the clear relationship between the strength and mechanisms of sexual selection and the degree of dimorphism. Here, we examine body size dimorphism across ontogeny in male and female rhesus macaques to assess whether it is primarily achieved via bimaturism as predicted by a polygynandrous mating system, faster male growth indicating polygyny, or both. We measured body mass in a cross-sectional sample of 364 free-ranging rhesus macaques from Cayo Santiago, Puerto Rico to investigate size dimorphism: 1) across the lifespan; and 2) as an outcome of sex-specific growth strategies, including: a) age of maturation; b) growth rate; and c) total growth duration, using regression models fit to sex-specific developmental curves. Significant body size dimorphism was observed by prime reproductive age with males 1.51 times the size of females. Larger male size resulted from a later age of maturation (males: 6.8-7.8 years versus females: 5.5-6.5 years; logistic model) and elevated growth velocity through the pre-prime period (LOESS model). Though males grew to larger sizes overall, females maintained adult size for longer before senescence (quadratic model). The ontogeny of size dimorphism in rhesus macaques is achieved by bimaturism and a faster male growth rate. Our results provide new data for understanding the development and complexities of primate dimorphism.

Origin of the Human Soul: Making Sense of Emotional Fossils (trans. by Andrey Korchevskiy)

That humans evolved to be hyper-cooperative has always been problematic for the Darwinian view of evolution: a struggle among individuals for scarce resources. The most fundamental fossil findings are consistent with the proposal that the appearance of humans 6 million years ago represents a rare major biological transition. For the first time, individual mammals (humans) began dividing and coordinating their functional activities while assembling into organism-like groups. The refinement of this collective capacity for teamwork is the decisive human adaptation and constitutes our core human instincts evolved over millions of years, referred to as the “old mind.” Our own Homo sapiens species appeared 300,000 years ago. Because the evolutionary mechanisms of sexual selection and group selection became predominant, 1) cultural evolution, 2) the rise of economic behavior, 3) chronic war, and 4) mental illness resulted. The major mental illnesses are viewed as “emotional fossils” that provide insight into the evolutionary development of our emotions and motivations. The symptoms of bipolar disorder reflect the breakdown of instincts evolved by sexual selection for the benefits of cohesion among groups. The symptoms of schizophrenia reflect the breakdown of instincts evolved by group selection for the benefits of groups prevailing in competition with each other. These often-disruptive instincts constitute our “new mind” that seeks equilibrium with our old mind, which persists as the humanizing legacy of collective functioning refined through the ages by our hominin ancestors and now experienced as our innermost soul.

Decoupled Acoustic and Visual Components in the Multimodal Signals of the Common Cuckoo (Cuculus canorus)

Because of its parasitic habits, reproduction costs of the common cuckoo (Cuculus canorus) are mostly spent in pre-laying activities. Female costs are limited to searching host nests and laying eggs, whereas, males spend time in performing intense vocal displays, possibly with territorial purpose. This last aspect, together with a sexual plumage dimorphism, points to both intra- and inter-sexual selections operating within this species. One element triggering sexual selection is a differential fitness accrued by different phenotypes. Before analyzing possible sexual selection mechanisms operating in cuckoos, it is therefore necessary to verify whether there is a variability among male secondary characters by describing and quantifying them. Here we aimed to quantitatively characterize the main two potential candidates of sexual selection traits, i.e., calls and displays, shown by males at perches. During the 2019 breeding season, in a site within the Po Plain, we both audio and video recorded cuckoo males at five different perches. We analyzed acoustic variables as well as display sequences searching for potential correlations. We found a significant variation among calls that could be clustered into four vocal types. We also found that no visual displays were associated with vocal displays; cuckoo males were either vocal and motionless or soundless and active. We discuss our results under the perspective of the potential value of sexual selection in brood parasites and its role in its parasitic habit.

Selection on genes associated with the evolution of divergent life histories: Gamete recognition or something else?

Gamete compatibility, and fertilization success, is mediated by gamete-recognition genes (GRGs) that are expected to show genetic evidence of a response to sexual selection associated with mating system traits. Changes in the strength of sexual selection can arise from the resolution of sperm competition among males, sexual conflicts of interest between males and females, or other mechanisms of sexual selection. To assess these expectations, we compared patterns of episodic diversifying selection among genes expressed in the gonads of Cryptasterina pentagona and C. hystera, which recently speciated and have evolved different mating systems (gonochoric or hermaphroditic), modes of fertilization (outcrossing or selfing), and dispersal (planktonic larvae or internal brooding). Cryptasterina spp. inhabit the upper intertidal of the coast of Queensland and coral islands of the Great Barrier Reef. We found some evidence for positive selection on a GRG in the outcrossing C. pentagona, and we found evidence of loss of gene function in a GRG of the self-fertilizing C. hystera. The modification or loss of gene functionality may be evidence of relaxed selection on some aspects of gamete interaction in C. hystera. In addition to these genes involved in gamete interactions, we also found genes under selection linked to abiotic stress, chromosomal regulation, polyspermy, and egg-laying. We interpret those results as possible evidence that Cryptasterina spp. with different mating systems may have been adapting in divergent ways to oxidative stress or other factors associated with reproduction in the physiologically challenging environment of the high intertidal. RESEARCH HIGHLIGHTS: Recent speciation between two sea stars was unlikely the result of selection on gamete-recognition genes annotated in this study. Instead, our results point to selection on genes linked to the intertidal environment and reproduction.