SEXUAL CONFLICT AND SEXUAL SELECTION: MEASURING ANTAGONISTIC COEVOLUTION

Abstract Arnqvist (2004) raises some concerns with several of the points made by Pizzari and Snook (2003) on the study of sexually antagonistic coevolution (SAC) generated by sexual conflict, arguing that: (1) sexual conflict cannot be expressed in terms of average male and female fitness; (2) our criticism of current experimental approaches, particularly interpopulation crosses, is unjustified; and (3) the alternative experimental approach we proposed is problematic. Here we discuss and respond to these criticisms by: (1) clarifying that we can distinguish between SAC and mutualistic sexual coevolution by measuring changes in the average fitness of the reproducing subsamples of males and females of a population across generations, (2) maintaining that testing SAC using interpopulation crosses is undermined by the lack of a priori knowledge of what traits mediate SAC across isolated populations, and (3) reinforcing the advantages of our experimental approach to distinguish between sexually mutualistic and antagonistic selection.     

INTERACTION-INDEPENDENT SEXUAL SELECTION AND THE MECHANISMS OF SEXUAL SELECTION

Darwin identified explicitly two types of sexual selection, male contests (combat and displays) and female choice, and he devoted the overwhelming majority of his examples to traits that influence the outcome of these interactions. Subsequent treatments of sexual selection have emphasized the importance of intra- and intersexual interactions as sources of sexual selection. However, many traits that are important determinants of mating success influence mating success without necessarily affecting the outcome of intra- and intersexual interactions. Here, I argue that traits can be subject to sexual selection even if they do not affect the outcome of intra- and intersexual interactions. I distinguish two types of sexual selection, interaction-independent and interaction-dependent selection, based on whether variance in mating success is the result of trait-dependent outcomes of interactions between conspecifics. I then use this distinction to construct a framework for classifying types of sexual selection that unifies and expands previously proposed frameworks. Finally, I outline several implications that the concept of interaction-independent sexual selection has for the general theory of sexual selection.     

SEXUAL DIMORPHISM IN CYPRAEIDAE

EVIDENCE of sexual dimorphism has been found in two species,Cypraeagracilis Gaskoin and Umbilia hesitata Iredale. In theformer the observed difference lies in the colour of the livinganimals, and in the latter in the length of the shell, the malebeing the longer. (Received 10 June 1960;     

SIGNALING EFFICACY DRIVES THE EVOLUTION OF LARGER SEXUAL ORNAMENTS BY SEXUAL SELECTION

Why are there so few small secondary sexual characters? Theoretical models predict that sexual selection should lead to reduction as often as exaggeration, and yet we mainly associate secondary sexual ornaments with exaggerated features such as the peacock's tail. We review the literature on mate choice experiments for evidence of reduced sexual traits. This shows that reduced ornamentation is effectively impossible in certain types of ornamental traits (behavioral, pheromonal, or color‐based traits, and morphological ornaments for which the natural selection optimum is no trait), but that there are many examples of morphological traits that would permit reduction. Yet small sexual traits are very rarely seen. We analyze a simple mathematical model of Fisher's runaway process (the null model for sexual selection). Our analysis shows that the imbalance cannot be wholly explained by larger ornaments being less costly than smaller ornaments, nor by preferences for larger ornaments being less costly than preferences for smaller ornaments. Instead, we suggest that asymmetry in signaling efficacy limits runaway to trait exaggeration.     

SEXUAL DIMORPHISM IN MAMMALS

1. Life expectancy and mortality rates from diseases arising in various organs vary with sex because of differential exposure to external hazards and because of essential differences between males and females in aspects not directly connected with reproduction. This review attempts to collate data about the structural and functional dimorphism of mammals exclusive of the genital organs and psychological aspects. 2. The primary sex ratio is not certain and like the secondary and tertiary may vary with species. In many mammals more males are aborted and born than females. Later a higher mortality of males, due to sex-linked congenital diseases and greater exposure to external hazards, shifts the balance in favour of females at the time of sexual maturity. The average life span of females is longer than that of males, except in hamsters and in inbred strains of mice with a high incidence of mammary tumours. 3. Chromosomes as well as gonadal hormones are responsible for the development of male and female characteristics. The Y-chromosome initiates the differentiation of the testis, but gonadal hormones control the subsequent differentiation of the genital tract and other organs. In embryos the testicular secretion precedes that of the ovary. The Y-chromosome is devoid of, but the X-chromosome retains structural genes. The random heterochromatization of a paternal or a maternal X-chromosome in the somatic cells of female embryos equalizes the genetic information for both sexes and produces a mosaicism of female somatic cells except in the kangaroo where the paternal X-chromosome is selectively inactivated. Deficient genes on the X-chromosome become manifest in hemizygous males, in homozygous females and can be detected in heterozygous women in half of the somatic cell population in some conditions. 4. The testis grows faster than the ovary and starts to secrete earlier, but the maturation of female gonocytes precedes that of males. Spermatogenesis starts at puberty and is maintained throughout life, while multiplication of oogonia ceases in the perinatal period (except in lemurs), when the stage of the first meiotic division is reached. The stock of oocytes dwindles during life. 5. In many mammals the male grows faster than the female before and after birth, but is less mature. Puberty tends to start earlier in females and the associated growth spurt does not last as long as in males. Testosterone has a direct anabolic effect, promotes growth and delays differentiation. Oestrogens are considered katabolic, but promote growth indirectly by stimulating the production of growth hormone in the pituitary. Progesterone has an anabolic and slight androgenic effect. 6. A female pattern of differentiation of the hypothalamus, the pituitary and the pineal gland, manifested at puberty by cyclical activities of the reproductive organs requires the absence of androgens during a critical phase of ante- or perinatal development. Oestrogens given to males at that period produce effects similar to castration. Antiandrogens induce in males a cyclical pattern of function in the hypothalamus and the pituitary, enlargement of the breasts and formation of nipples in the rat and a female type of sexual behaviour. There is no complete sex reversal in mammals comparable to that of fish and amphibians. 7. With some exceptions (hamsters, rabbits, guinea-pigs) males are larger than females. Gender differences in weight of organs and in other parameters must be assessed as proportion to male or female weight, surface and activities. The relatively greater amount of fat in female and of connective tissue in male organs in relation to the active parenchyma complicate comparisons. 8. The head and shoulder region is proportionately larger in males and the pelvic region in females. Men and male mice have heavier bones, muscles, hearts, lungs, salivary glands, kidneys and gonads in proportion to body weight, while females have proportionately heavier brains, livers, spleens, adrenals, thymus, stomach and fat deposits. 9. The basal metabolic rate in women is lower than in males. A great variety of metabolic parameters, levels of enzyme activity, location of fat deposits, sensitivity to drugs is sexually dimorphic and responsive to the action of androgens, oestrogens and progestagens. 10. Males tend to have more red blood corpuscles, haemoglobin and erythropoietin per unit volume of blood than women, cows, mares, sows, bitches, female cats and hamsters, but there is no sex difference in this respect in rats, rabbits, goats or sheep. Females tend to have more granulocytes and a proportionately larger lymphomyeloid complex (bone marrow, spleen, thymus, lymph nodes and lymphoepithelial tissues) and greater immunological competence than males. The cortical epithelium of the thymus in mice and rats is sexually dimorphic, responsive to castration and treatment with sex hormones and varies with the oestrous cycle. 11. The kidney is proportionately larger in male mice, rats, cats and dogs, is reduced by castration and enlarged by treatment with testosterone. The kidneys of hamsters and guinea-pigs do not differ in size with sex, nor do they respond to castration or to androgens. The proportion of tubules to glomeruli is greater in the male than the female kidney. The tubular mass increases with androgenic medication, but not the juxtaglomerular apparatus. The parietal epithelium of Bowman's capsule, the histochemistry of the kidney and the composition of the urine vary with gender and respond to sex hormones according to species and strain. The bladder of male mice is proportionately larger than that of females. Some pheromones are present in the bladder urine of intact male mice and of spayed females given testosterone, but absent from that of castrated males. 12. Boars, male elephants, mastodons, horses, deer and monkeys have larger canines than the females. The submaxillary gland of male mice, rats and pigs is proportionately larger than in females, but smaller in hamsters. The proportion of mucous to serous acinar cells in female rodents is greater than in males; female hamsters produce more sialic acid. The secretory tubules of male rats and mice are larger than in females and produce a nerve- and an epidermal-growth factor. Apart from amylase the levels of enzyme activity vary with sex. The liver is sexually dimorphic as regards size, content and metabolism of glycogen, fat, vitamin A, levels of enzymatic activity, phagocytic activity and in its response to castration, sex hormones, to toxic agents, drugs and carcinogens. Sex hormones affect the production of insulin by the pancreas in vivo and in vitro. 13. The male larynx which enlarges and induces voice changes in many mammals at puberty or the onset of the breeding season, is affected by castration and by sex hormones. Male lungs are proportionately larger than female ones with a greater vital and maximal respiratory capacity. Breathing rate and manner varies with sex and is related to differences in the muscular development of the diaphragm. 14. The epidermis and dermis of males are thicker, but the subcutis thinner than in females. The skin is sexually dimorphic in respect of dermatoglyphics, the replacement of vellus by terminal hair and pigmentation of specific regions, the colour of the face and of the sexual skin in monkeys, the development of antlers and horns. The synchrony of the hair cycle and the growth wave of the hair coat in mice and rats depend on the sex of the animals. The X-chromosome mosaicism in the hair follicles of female mice accounts for the mosaicism in pigmentation. Apart from a genetic disorder, the sweat glands are not sexually dimorphic, but the apocrine, the sebaceous glands and their specialized forms are. The embryonic development of mammary glands depends on the absence of androgens and can be induced in male rats and guinea-pigs by antiandrogens. 15. An intact cerebral cortex is necessary for the performance of reproductive functions in male, but not in female rats, cats, rabbits and guinea-pigs. Removal of the olfactory bulb impairs reproduction in female, but not in male mice. Pinealectomy prevents the testicular atrophy of hamsters kept in the dark. The reproductive cycles in females are regulated by the hypothalamus through the control of the ratio of FSH to LH release in the pituitary. This in turn acts on the ovary and thus affects the activity of the thyroid, thymus and lung. In males FSH and LH act synergistically and their secretion is not controlled separately. Oestrogens are more effective than androgens in inhibiting pituitary functions. Sexual dimorphism in cytology, enzyme levels and oestrogen-binding is manifest in the preoptic area, the hypothalamus and the nucleus medialis amygdalae. The female brain is proportionately larger than the male with equal relative amounts of grey and white matter, but a bigger hypothalamic-pituitary-pineal complex. The pineal gland is more prone to tumour formation in boys than in girls and retains its cellularity longer in women than in men. Colour blindness is manifested less in heterozygous women than in hemizygous men. Mature women are more sensitive to the smell of synthetic musk than girls or men. Male rats and mice are more susceptible to audiogenic seizures than females. 16. The activity of the thyroid gland varies at different phases of the oestrous cycle in rats, mice and guinea-pigs. Female mice release more thyroid hormone into the blood than males or spayed animals. Oestrogens increase the level of thyroxin-binding protein. The concentration of TSH in the blood of mature women is double that of men and of menopausal women. The incidence of non-endemic thyroid disorders in women considerably exceeds that in men. 17. The adrenals of females are much larger than those of males except in hamsters. The gland of the female mouse contains more lipid than that of the male. The juxtamedullary X-zone of mice involutes at puberty in males and during the first pregnancy in females. Castration induces an X-zone in male mice, voles, hamsters and cats and an enlargement without stratification in rats. ACTH controls the secretion of glucocorticoids and since its formation is promoted by oestrogens and inhibited by androgens, sex hormones influence indirectly the size and activity of the adrenal cortex. Hepatic inactivation of glucocorticoids is 3 to 10 times greater in intact females than in males. 18. The implications of species variations in sexual dimorphism for the survival and the evolution of mammals are discussed.     

SEX RATIO DRIVE PROMOTES SEXUAL CONFLICT AND SEXUAL COEVOLUTION IN THE FLY DROSOPHILA PSEUDOOBSCURA

Selfish genetic elements occur in all living organisms and often cause reduced fertility and sperm competitive ability in males. In the fruit fly Drosophila pseudoobscura, the presence of a sex‐ratio distorting X‐chromosome meiotic driver Sex Ratio (SR) has been shown to promote the evolution of increased female remating rates in laboratory populations. This is favored because it promotes sperm competition, which decreases the risk to females of producing highly female‐biased broods and to their offspring of inheriting the selfish gene. Here, we show that non‐SR males in these SR populations evolved an increased ability to suppress female remating in response to the higher female remating rates, indicating male–female coevolution. This occurred even though SR was rare in the populations. This was further supported by a correlation between females’ remating propensity and males’ ability to suppress female remating across populations. Thus SR can generate sexual conflict over female remating rate between females and the noncarrier males that make up the majority of the males, promoting evolution of increased ability of males to suppress female remating.     

THE FUSION OF SEXUAL NUCLEI

A classification scheme is proposed for the types of sexual nuclear fusion that occur in eukaryotes. The two main classes are envelope fusion and envelope vesiculation and each is further divided into subclasses. The formation of sexual nuclei (pronuclei) has been detailed in representatives from various phyla, but is best understood in animals, in which the development of male and female pronuclei differs in some respects. The only characterized cytoplasmic mediator of pronuclear movement are microtubules. Groups of eukaryotes can be classified according to the type of nuclear fusion they reveal. Envelope fusion occurs in animals whose eggs are fertilized at the pronuclear stage, and in all plants, fungi, protozoa and algae studied to date. Ultrastructural details of envelope fusion have shown variations that are classified in our scheme as direct and indirect, the latter being restricted to the plant kingdom. Envelope vesiculation only occurs in animals, in which it is the most common means of nuclear fusion. Four subclasses can be defined according to the timing of the vesiculation of the nuclear envelopes, and the extent of envelope surface projections prior to fusion. The amount of work reported on the controlling mechanisms of nuclear fusion has been limited, but some evidence of genetic control has been provided, particularly in fungi. Evidence is presented to indicate that the control of the fusion competence of nuclei is a negative one. This review of the information available on nuclear fusion points out the need for extensive future comparative studies if this important process is to be better understood.     

MUTATIONAL MELTDOWNS IN SEXUAL POPULATIONS

Although it is widely acknowledged that the gradual accumulation of mildly deleterious mutations is an important source of extinction for asexual populations, it is generally assumed that this process is of little relevance to sexual species. Here we present results, based on computer simulations and supported by analytical approximations, that indicate that mutation accumulation in small, random-mating monoecious populations can lead to mean extinction times less than a few hundred to a few thousand generations. Unlike the situation in obligate asexuals in which the mean time to extinction (t?_e) increases more slowly than linearly with the population carrying capacity (K), t?_e increases approximately exponentially with K in outcrossing sexual populations. The mean time to extinction for obligately selfing populations is shown to be equivalent to that for asexual populations of the same size, but with half the mutation rate and twice the mutational effect; this suggests that obligate selfing, like obligate asexuality, is inviable as a long-term reproductive strategy. Under all mating systems, the mean time to extinction increases relatively slowly with the logarithm of fecundity, and mutations with intermediate effects (similar to those observed empirically) cause the greatest risk of extinction. Because our analyses ignore sources of demographic and environmental stochasticity, which have synergistic effects that exacerbate the accumulation of deleterious mutations, our results should yield liberal upper bounds to the mean time to extinction caused by mutational degradation. Thus, deleterious mutation accumulation cannot be ruled out generally as a significant source of extinction vulnerability in small sexual populations or as a selective force influencing mating-system evolution.