Interactions between the sexes: new perspectives on sexual selection and reproductive isolation

Understanding the processes underlying the origin of new species is a fundamental problem in evolutionary research. Whilst it has long been recognised that closely related taxa often differ markedly in reproductive characteristics, only relatively recently has sexual selection been evoked as a key promoter of speciation through its ability to generate reproductive isolation (RI). Sexual selection potentially can influence the probability that individuals from the same or different populations will reproduce successfully since it shapes precisely those traits involved in mating and reproduction. If reproductive characters diverge along different trajectories, then sexual selection can impact on the evolution of reproductive barriers operating both before and after mating. In this perspective, we consider some new advances in our understanding of the coevolution of male and female sexual signals and receptors and suggest how these developments may provide heretofore neglected insights into the mechanisms by which isolating barriers may emerge. Specifically, we explore how selfish genetic elements (SGEs) can mediate pre- and post-copulatory mate choice, thereby influencing gene flow and ultimately population divergence; we examine evidence from studies of intracellular sperm–egg interactions and propose that intracellular gametic incompatibilities may arise after sperm entry into the egg, and thus contribute to RI; we review findings from genomic studies demonstrating rapid, adaptive evolution of reproductive genes in both sexes and discuss whether such changes are causal in determining RI or simply associated with it; and finally, we consider genetic, developmental and functional mechanisms that might constrain reproductive trait diversification, thereby limiting the scope for reproductive barriers to arise via sexual selection. We hope to stimulate work that will further the understanding of the role sexual selection plays in generating RI and ultimately speciation.     

Chromosome-scale genome assembly of the African giant pouched rat (Cricetomys ansorgei) and evolutionary analysis reveals evidence of olfactory specialization

The Southern giant pouched rat, Cricetomys ansorgei, is a large rodent best known for its ability to detect landmines using its impressive sense of smell. Their powerful chemosensory abilities enable subtle discrimination of chemical social signals, and female pouched rats demonstrate a unique reproductive physiology hypothesized to be mediated by pheromonal mechanisms. Thus, C. ansorgei represents a novel mammalian model for chemosensory physiology, social behavior, and pheromonal control of reproductive physiology. We present the first chromosome-scale genomic sequence of the pouched rat encoding 22,671 protein coding genes, including 1571 olfactory receptors, and provide a glance into the evolutionary history of this species. Functional enrichment analysis reveals genetic expansions specific to the pouched rat are enriched for functions related to olfactory specialization. Overall, this assembly is of reference-quality, and will serve as a useful and informative genomic sequence on which we can confidently base future molecular research involving the pouched rat.     

Estrogen and endogenous opioids regulate CCK in reproductive circuits.

This review focuses on the interaction of estrogen with the cholecystokinin (CCK) and endogenous opioid peptide systems in the medial preoptic nucleus, and how these interactions result in alterations of a stereotypic female reproductive behavior--lordosis. The medial preoptic nucleus is an integral part of a circuit controlling lordosis that extends from the limbic system through the hypothalamus. Estrogen alters the integration of sensory information in the circuit that results in the display of sexually receptive behavior. Estrogen determines the activity of CCK and endogenous opioid peptide systems through regulation of expression, release and interaction with specific receptors. Studies of each system individually have indicated that they are pivotal to the expression of lordosis. Recent studies demonstrate an estrogen-dependent interaction between endogenous opioid and CCK systems that control reproductive behavior.     

Release of orphanin FQ/nociceptin in the medial preoptic nucleus and ventromedial nucleus of the hypothalamus facilitates lordosis

Opioid regulation of reproduction has been widely studied. However, the role of opioid receptor-like 1 receptor (NOP; also referred to as ORL-1 and OP4) and its endogenous ligand orphanin FQ/nociceptin (OFQ/N) have received less attention despite their extensive distribution throughout nuclei of the limbic-hypothalamic system, a circuit that regulates reproductive behavior in the female rat. Significantly, the expression of both receptor and ligand is regulated in a number of these nuclei by estradiol and progesterone. Activation of NOP in the ventromedial nucleus of the hypothalamus (VMH) of estradiol-primed nonreceptive female rats facilitates lordosis. NOPs are also expressed in the medial preoptic nucleus (MPN), however, their roles in reproductive behavior have not been studied. The present experiments examined the role of NOP in the regulation of lordosis in the MPN and tested whether endogenous OFQ/N in the MPN and VMH mediates reproductive behavior. Activation of NOP by microinfusion of OFQ/N in the MPN facilitated lordosis in estradiol-primed sexually nonreceptive female rats. Passive immunoneutralization of OFQ/N in either the MPN or the VMH reduced lordosis in estradiol-primed females, but had no effect on lordosis in estradiol+progesterone-primed sexually receptive rats. These studies suggest that OFQ/N has a central role in estradiol-only induced sexual receptivity, and that progesterone appears to involve additional circuits that mediate estradiol+progesterone sexual receptivity.     

雌性动物多次交配行为的机制及进化

雌性动物的后代数量不可能超过她的卵子数。在理论上, 一个生殖季节内, 一次或几次交配就足够使雌性所有卵子受精, 最大化其生殖潜能。但与理论预测相反, 许多物种的雌性经常与同一个或多个雄性发生多次交配。交配通常要付出较高的代价, 所以很难理解为什么雌性动物要反复进行多次交配。本文综述了解释此行为的一些适应性和非适应性假说。从获得直接收益和间接收益二个角度介绍了适应性假说。直接收益主要包括求偶喂食和“彩礼”、受精保证、亲代抚育、生殖刺激和护卫交配权等5 个方面。还着重介绍了多次交配对雌性后代的间接遗传受益, 即获得优质基因、提高后代遗传多样性和遗传互补性3 个假说。非适应性假说包括了遗传相关假说和顺从雄性行为假说。     

Hormonal control of female sexual behavior in the rat

Graded amounts of estradiol benzoate (ranging from 0.48 to 500 μg/kg) were administered to ovariectomized, adrenalectomized female rats in order to analyze the effects of estrogen on the qualitative and quantitative aspects of female reproductive behavior in this species. The interaction of hormone dose and copulatory stimulation was also investigated. In this study, soliciting behavior and lordosis responses were broken down into subcategories. There were three main results. First, it was found that the responses were hierarchically arranged such that, with increasing doses of hormone, the common elements of sexual responding appeared in the same order across individual females. Second, the chronic endocrine background of the female influenced the degree of her receptivity following an acute injection of estrogen. Third, repeated elicitation of lordosis by copulatory stimulation facilitated the subsequent occurrence of lordosis.     

Effect of thyroid hormone administration on estrogen-induced sex behavior in female mice

Effects of thyroid hormones on reproductive processes have been described in sheep, birds, and rats. To extend this subject to mice for eventual analysis with genetically modified animals, we looked for effects of thyroid hormone treatment on lordosis behavior of ovariectomized estrogen-treated female mice. High doses of thyroid hormones reduced lordosis behavior. Since we could not explain this result by pharmacokinetic or peripheral effects, we infer that it worked by a central mechanism. Future investigations must determine whether endogenous fluctuations within the thyroid's normal physiological range have any behavioral effects.     

Neuroendocrine regulation of estrous behavior in the rabbit: similarities and differences with the rat

In this review, we compare the neuroendocrine control of estrous behavior in the rabbit, a reflex ovulator, and the rat, a more commonly studied spontaneous ovulator. Although the hormonal control of estrous behavior in both species is similar, notable differences include the absence of a stimulatory effect of progesterone (P) on sexual behavior in the rabbit and the retention of sexual behavior in a substantial proportion of female rabbits after ovariectomy. The ventrolateral component of the ventromedial hypothalamus (VMH) and an adjacent region caudal to it appear to be critical estrogen (E)-responsive regions for lordosis in the rat and rabbit, respectively. In both species the effects of E and P are largely mediated by the genomic action of their receptors (ER and PR), and in both species E similarly regulates the expression of these receptors. The prolonged, E-stimulated estrous of the rabbit is terminated after mating by unknown mechanisms, while the brief estrous of the rat is triggered by the proestrous peak of P and terminated by both the decline in P and the downregulation of hypothalamic PR. In both species, P most likely inhibits estrous behavior during pregnancy, and postpartum estrous may be triggered by a stimulatory effect of E coinciding with the withdrawal of P-mediated inhibition. Estrous behavior is inhibited in both species during lactation, most likely by the suckling-induced inhibition of gonadotropin secretion. This comparative approach can reveal neuroendocrine mechanisms underlying estrous behavior that are common to all mammals, while highlighting evolutionary adaptations unique to each species.     

Reproductive development and induced estrus in the prepubertal hamster

During puberty ovarian, hypothalamic, and behavioral processes become coordinated to foster reproductive success. The present study investigated the lordosis capability as a possible limiting factor in the initiation of puberty.Intact and castrate female golden hamsters at 18 to 28 days of age were found capable of demonstrating an adult-like lordosis response when primed with estrogen and progesterone. This is before ovulation or hypothalamic cyclicity is usual. In the hamster, then, estrous behavior is one of the first reproductive capabilities to mature. Early ovariectomy seems to delay the development of the tissues mediating lordosis. Ovarian maturation is probably the crucial limiting factor for puberty in the hamster.     

Signatures of hybridization and speciation in genomic patterns of ancestry*

Genomes sampled from hybrid zones between nascent species provide important clues into the speciation process. With advances in genome sequencing and single nucleotide polymorphism (SNP) genotyping, it is now feasible to measure variation in gene flow with high genomic resolution. This progress motivates the development of conceptual and analytical frameworks for hybrid zones that complement well‐established cline approaches. We extend the perspective that genomic distributions of ancestry are sensitive indicators of hybridization history. We use simulations to examine the behavior of the number of ancestry junctions—a simple summary of genomic patterns—in hybrid zones under increasingly realistic scenarios. Neutral simulations revealed that ancestry junction number is shaped by population structure, migration rate, and population size. Modeling multiple genetic architectures of hybrid dysfunction, with an emphasis on epistatic hybrid incompatibilities, showed that selection reduces junction number near loci that confer reproductive barriers. The magnitude of this signature was affected by the form of selection, dominance, and genomic location (autosome vs. sex chromosome) of incompatible loci. Our results suggest that researchers can identify loci involved in reproductive isolation by scanning hybrid genomes for local reductions in junction number. We outline necessary directions for future theory and method development to realize this goal.     

Reproductive barrier and genomic imprinting in the endosperm of flowering plants

In flowering plants, success or failure of seed development is determined by various genetic mechanisms. During sexual reproduction, double fertilization produces the embryo and endosperm, which both contain maternally and paternally derived genomes. In endosperm, a reproductive barrier is often observed in inter-specific crosses. Endosperm is a tissue that provides nourishment for the embryo within the seed, in a similar fashion to the placenta of mammals, and for the young seedling after germination. This review considers the relationship between the reproductive barrier in endosperm and genomic imprinting. Genomic imprinting is an epigenetic mechanism that results in mono-allelic gene expression that is parent-of-origin dependent. In Arabidopsis, recent studies of several imprinted gene loci have identified the epigenetic mechanisms that determine genomic imprinting. A crucial feature of genomic imprinting is that the maternally and paternally derived imprinted genes must carry some form of differential mark, usually DNA methylation and/or histone modification. Although the epigenetic marks should be complementary on maternally and paternally imprinted genes within a single species, it is possible that neither the patterns of epigenetic marks nor expression of imprinted genes are the same in different species. Moreover, in hybrid endosperm, the regulation of expression of imprinted genes can be affected by upstream regulatory mechanisms in the male and female gametophytes. Species-specific variations in epigenetic marks, the copy number of imprinted genes, and the epigenetic regulation of imprinted genes in hybrids might all play a role in the reproductive barriers observed in the endosperm of interspecific and interploidy crosses. These predicted molecular mechanisms might be related to earlier models such as the "endosperm balance number" (EBN) and "polar nuclei activation" (PNA) hypotheses.     

Atrazine and reproductive function: mode and mechanism of action studies

Atrazine, a chlorotriazine herbicide, is used to control annual grasses and broadleaf weeds. In this review, we summarize our laboratory's work evaluating the neuroendocrine toxicity of atrazine (and related chlorotriazines) from an historic perspective. We provide the rationale for our work as we have endeavored to determine: 1) the underlying reproductive changes leading to the development of mammary gland tumors in the atrazine-exposed female rat; 2) the cascade of physiological events that are responsible for these changes (i.e., the mode of action for mammary tumors); 3) the potential cellular mechanisms involving adverse effects of atrazine; and 4) the range of reproductive alterations associated with this pesticide.     

Comparative Analyses of Reproductive Structures in Harvestmen (Opiliones) Reveal Multiple Transitions from Courtship to Precopulatory Antagonism

Explaining the rapid, species-specific diversification of reproductive structures and behaviors is a long-standing goal of evolutionary biology, with recent research tending to attribute reproductive phenotypes to the evolutionary mechanisms of female mate choice or intersexual conflict. Progress in understanding these and other possible mechanisms depends, in part, on reconstructing the direction, frequency and relative timing of phenotypic evolution of male and female structures in species-rich clades. Here we examine evolution of reproductive structures in the leiobunine harvestmen or “daddy long-legs” of eastern North America, a monophyletic group that includes species in which males court females using nuptial gifts and other species that are equipped for apparent precopulatory antagonism (i.e., males with long, hardened penes and females with sclerotized pregenital barriers). We used parsimony- and Bayesian likelihood-based analyses to reconstruct character evolution in categorical reproductive traits and found that losses of ancestral gift-bearing penile sacs are strongly associated with gains of female pregenital barriers. In most cases, both events occur on the same internal branch of the phylogeny. These coevolutionary changes occurred at least four times, resulting in clade-specific designs in the penis and pregenital barrier. The discovery of convergent origins and/or enhancements of apparent precopulatory antagonism among closely related species offers an unusual opportunity to investigate how major changes in reproductive morphology have occurred. We propose new hypotheses that attribute these enhancements to changes in ecology or life history that reduce the duration of breeding seasons, an association that is consistent with female choice, sexual conflict, and/or an alternative evolutionary mechanism.     

孕酮受体介导哺乳动物雌性生殖活动的分子机理

孕酮作为一种甾体激素,在哺乳动物雌性生殖活动的调控中起着关键作用。孕酮的生理功能依赖于核孕酮受体介导的基因组效应和膜孕酮受体介导的非基因组效应,这两种效应共同介导了孕酮在各种雌性生殖活动中的不同作用,包括排卵、胚胎植入、妊娠维持、分娩启动和乳腺发育等。近年来,通过基因芯片技术筛选出大量的孕酮下游靶基因,但至今未能在这些基因的启动子区域上找到传统意义上的孕酮响应元件,故推测核孕酮受体调节下游靶基因转录活动的方式可能不同于传统的类固醇核受体。基于目前最新的研究成果,文章综述了在哺乳动物雌性生殖活动中,孕酮受体介导各种生理效应的分子机理。     

Looking for sexual selection in the female brain

Female mate choice behaviour has significant evolutionary consequences, yet its mechanistic origins are not fully understood. Recent studies of female sensory systems have made great strides in identifying internal mechanisms governing female preferences. Only recently, however, have we begun to identify the dynamic genomic response associated with mate choice behaviour. Poeciliids provide a powerful comparative system to examine genomic responses governing mate choice and female preference behaviour, given the great range of mating systems: from female mate choice taxa with ornamental courting males to species lacking male ornamentation and exhibiting only male coercion. Furthermore, they exhibit laboratory-tractable preference responses without sexual contact that are decoupled from reproductive state, allowing investigators to isolate mechanisms in the brain without physiological confounds. Early investigations with poeciliid species (Xiphophorus nigrensis and Gambusia affinis) have identified putative candidate genes associated with female preference response and highlight a possible genomic pathway underlying female social interactions with males linked functionally with synaptic plasticity and learning processes. This network is positively correlated with female preference behaviour in the female mate choice species, but appears inhibited in the male coercive species. This behavioural genomics approach provides opportunity to elucidate the fundamental building blocks, and evolutionary dynamics, of sexual selection.     

Why dominants do not consistently attain high mating and reproductive success: A review of longitudinal Japanese macaque studies

There is wide interest in the effects of reproductive biology, mating partner preference, and rank on mating success (MS) and reproductive success (RS) in primates. In particular, theory stresses importance on the mechanisms for attaining RS. Most theory hedges on competitive ability and priority of access to resources, whether they be food or estrous females. However, the majority of data used in favor of such hypotheses come from relatively short-term studies. We review these hypotheses based on long-term data from provisioned and unprovisioned populations of Japanese macaques. Neither MS nor RS were consistently attained by high-ranking males and females. For males, female choice and mating partner preference is seen to over-ride most male-male competitive behaviors likely to affect MS and RS through priority of access to estrous females. Long-term mating patterns driven largely by female partner preferences, results in decreasing MS and RS for older higher-ranking males. The long-term trend for females to prefer less familiar or novel partners results in higher MS and RS for younger, middle-ranking males. The effects of this vary according to troop size and the duration of male tenure. For females, no consistent trend was recognized for rank related RS in either provisioned or unprovisioned troops. Non-reproductive mating may provide differential benefit to high-ranking females for access to limited food resources in some habitats but overall the relationship was inconclusive. Distribution and defendability of food resource, rather than provisioning per se may be more important.     

Intracranial dialysis and microinfusion studies suggest that morphine may act in the ventromedial hypothalamus to inhibit female rat sexual behavior.

The present investigation examined the neural sites and mechanisms of opiate inhibition of female sexual behavior. Systemic administration of morphine (10 mg/kg) significantly reduced ovarian steroid-induced estrous behavior in female rats. This behavioral inhibition was prevented when the opiate receptor antagonist naloxone (5 mg/kg) was administered 30 min prior to morphine. Bilateral infusion of morphine directly into the ventromedial hypothalamus (VMH) also inhibited hormone-dependent estrous behavior for at least 2 hr. Furthermore, naloxone infusion into the VMH 20 min before behavior testing reduced the inhibitory effects of systemically administered morphine on lordosis. These results suggest that morphine may inhibit female sexual behavior by acting directly on the VMH, the primary site at which ovarian steroids facilitate this behavior. In a separate experiment we used in vivo brain microdialysis to test the hypothesis that morphine inhibits lordosis by interfering with norepinephrine (NE) neurotransmission in the VMH. In control rats, the onset of mating was associated with increased NE release in the VMH. Morphine-treated animals displayed neither behavioral estrus nor elevated NE release from the VMH when tested with stimulus males. These data are consistent with the hypothesis that morphine suppresses NE release in the VMH. Nevertheless, mechanisms other than or in addition to attenuation of hypothalamic NE release may contribute to the inhibitory effects of morphine on lordosis.     

Adaptiveness and adaptation

This essay is structured as follows. First, I describe the adaptationist program, or teleonomy, in biology. Second, I review the methodologies of this program. Third, I discuss the role that the environment of evolutionary adaptedness plays in the adaptationist program. Fourth, I argue that studies of the “adaptiveness” of human behavior have not been conceptually anchored in the adaptationist program. Fifth, I analyze two studies of adaptiveness and show why they neither test nor inspire novel hypotheses about the design of the human brain/mind. Finally, I conclude that the “adaptivist” approach to human behavior does not begin with well formed hypotheses about the design of human brain/mind mechanisms and that it consists of procedures that could not test such hypotheses if they were proposed.