Toward a New Sexual Selection Paradigm: Polyandry, Conflict and Incompatibility (Invited Article)

Darwin's recognition that male–male competition and female choice could favor the evolution of exaggerated male traits detrimental to survival set the stage for more than a century of theoretical and empirical work on sexual selection. While this Darwinian paradigm represents one of the most profound insights in biology, its preoccupation with sexual selection as a directional evolutionary force acting on males has diverted attention away from the selective processes acting on females. Our understanding of female reproduction has been further confounded by discreet female mating tactics that have perpetuated the illusion of the monogamous female and masked the potential for conflict between the sexes. With advances in molecular techniques leading to the discovery that polyandry is a pervasive mating strategy, recognition of these shortcomings has brought the study of sexual selection to its current state of flux. In this paper, we suggest that progress in two key areas is critical to formulation of a more inclusive, sexual selection paradigm that adequately incorporates selection from the female perspective. First, we need to develop a better understanding of male × female and maternal × paternal genome interactions and the role that polyandry plays in providing females with non‐additive genetic benefits such as incompatibility avoidance. Consideration of these interaction effects influencing natural selection on females is important because they can complicate and even undermine directional sexual selection on males. Secondly, because antagonistic coevolution maintains a balance between opposing sides that obscures the conflict itself, many more experimental evolution studies and interventionist investigations (e.g. gene knockouts) are needed to tease apart male manipulative adaptations and female counter‐adaptations. It seems evident that the divisiveness and controversy that has plagued sexual selection theory since Darwin first proposed the idea has often stalled progress in this important field of evolutionary biology. What is now needed is a more pluralistic and integrative approach that considers natural as well as sexual selection acting on females, incorporates multiple sexual selection mechanisms, and exploits advances in physiology and molecular biology to understand the mechanisms through which males and females achieve reproductive success.     

Understanding Social Behaviour with the Help of Complexity Science (Invited Article)

In the study of complexity, a new kind of explanation has been developed for social behaviour. It shows how patterns of social behaviour can arise as a side‐effect of the interaction of individuals with their social or physical environment (e.g. by self‐organization). This development may influence our ideas about the direct causation and evolution of social behaviour. Furthermore, it may influence our theories about the integration of different traits. This new method has been made possible by the increase in computing power. It is now applied in many areas of science, such as physics, chemistry, sociology and economics. However, in zoology and anthropology it is still rare. The major aim of this paper is to make this method more generally accepted among behavioural scientists.     

Why Parental Sex Ratio Manipulation is Rare in Higher Vertebrates (Invited Article)

The debate over adaptive parental sex ratio adjustment in higher vertebrates appears neither to be resolvable by the current approach, nor does it necessarily make sense. It rests on the a priori supposition of parental manipulation, which is questioned here from first principle. It is considered an unlikely biological hypothesis if we extend our perspective to gametic and offspring optimal strategies, and to the potential mechanisms existing in the avian and mammalian reproductive systems. Evenness of primary sex ratios is expected to be optimal from the gametic point of view and is supposed here to be the more likely evolutionary outcome. Also, manipulations by sex-selective offspring mortality is argued to be unlikely as usually the benefits will be surpassed by the costs incurred. Furthermore, parents can adjust behavioural and energetic investment patterns to their offspring sex (ratio), thereby minimizing any costs of sex ratio control inability. Slight biases in offspring sex ratios are then viewed as resulting from physiological limitations ultimately relating to sex differences in embryonic development. Contrary to recent attempts to understand higher vertebrate sex ratio variation by further refinement of functional models (of parental optima) and data analysis, Bayesian logic precludes those approaches to gain useful new insights. To prove the basic assumption of parental manipulation, apart from defining gametic and offspring optima, the emphasis should lie on identifying control mechanisms by experimental verification.     

Timing of oviposition and reproductive skew in cobreeding female burying beetles (Nicrophorus vespilloides)

Burying beetles (genus Nicrophorus) are known for their elaborate parental care. Two or more conspecific females may reproduceon the same carcass, especially when the carcass is large.Here we present the results of experiments in which we observedpatterns of larval hatching and parental care in unmanipulatedcobreeders, manipulated hatching synchrony between cobreeders,and compared patterns of oviposition in cobreeding and single females. Our results show that in these cobreeding associations,one of the females may or may not monopolize the carcass duringthe period of larval hatching. We present evidence that ineither case, infanticide based on temporal cues constitutesan important proximate mechanism underlying the observed reductionin average reproductive success in cobreeding females. Femaleswith higher synchrony (i.e., greater overlap between their oviposition patterns) produce larger broods with lower reproductive skew.Cobreeding females oviposit later and less synchronously thansingle breeders. Such delayed oviposition may reduce the riskthat a female's larvae fall victim to cannibalistic acts committedby her cobreeder or maximize her own opportunity to selectivelykill her cobreeder's larvae.     

Indices of reproductive skew depend on average reproductive success

Several indices of reproductive skew, which quantify the degree of unequal partitioning of reproductive output among members in an animal society, have been proposed. Here we point out the drawbacks of these indices. The most serious problem is the dependence of the indices on mean reproductive success: skew values tend to be larger, as average numbers of offspring decrease, due to random sampling error in numbers of offspring. Thus it is difficult to compare societies with different average lifetime reproductive success using these indices, even though we have presented methods to calculate the expected reproductive skew caused by random sampling error, especially when average numbers of offspring are small, as is often the case with cooperatively breeding vertebrates. As an alternative, we propose using the spatial dispersion indices of population ecology (Morisita's index or its standardized version) for the measurement of reproductive skew. These indices are almost independent of average fecundity and have their own method of testing for random variation in offspring numbers. This revised version was published online in July 2006 with corrections to the Cover Date.     

Starving the competition: a proximate cause of reproductive skew in burying beetles (Nicrophorus vespilloides)

Proximate mechanisms underlying reproductive skew are obscure in many animals that breed communally. Here, we address causes of reproductive skew in brood-parasitic associations of burying beetles (Nicrophorus vespilloides). Male and female burying beetles feed and defend their larvae on buried carcasses. When several females locate the same small carcass, they engage in violent physical altercations. The subordinate then acts as an intraspecific brood parasite, laying eggs, but not providing care. The dominant female largely monopolizes access to the carcass; she alone provides parental care and her share of the brood is much larger than the subordinate's. On larger carcasses, subordinates have greater access to the carcass than on small ones, and reproductive skew is reduced. Differential fecundity, ovicide and larvicide have been suggested as causes of skew on small carcasses. Here, we report the results of the experiments pertaining to the first two of these potential mechanisms. Ovicide did not significantly contribute to reproductive skew on small carcasses, but differential fecundity did. Fecundity differences were due to dominance status, not body size per se. Fecundity differences disappeared when supplemental food was available, suggesting that reduced access to the carcass limits fecundity by causing nutritional deficiencies. Supplemental food prevented such nutritional deficiencies and allowed subordinates to produce as many eggs as dominants. Apparently, aggressive behaviour by dominants functions in the context of reproductive competition, limiting subordinate reproduction by preventing food intake on the carcass.     

A longitudinal analysis of reproductive skew in male rhesus macaques

One of the basic tenets of sexual selection is that male reproductive success should be large in polygynous species. Here, we analysed 6 years of molecular genetic data from a semi-free-ranging population of rhesus macaques (Macaca mulatta), using Nonac's B index, to assess the level of male reproductive skew in the study troop. On average, the top sire in each year produced 24% of the infants, while 71% of troop males sired no offspring at all. Consequently, 74% of infants had at least one paternal half-sibling in their own birth cohort. Reproductive success was greatest for high-ranking males, males who spent the whole mating season in the troop and males of 9-11 years of age. Heterozygosity for major histocompatibility complex (MHC) class II gene DQB1 was the strongest single predictor of male reproductive success. A negative relationship suggestive of female mate choice was noted between the B index and the proportion of extragroup paternities. Reproductive skew was not associated with relatedness among potential sires or with female cycle synchrony. We conclude that reproductive skew in male rhesus macaques is best accounted for by the 'limited-control' model, with multiple factors interacting to regulate individual reproductive output.     

Applied Stochastic Geometry: A Survey (Invited Paper)

The paper is a survey on some practical aspects of stochastic geometry in the sense of D. G. KENDALL 's and G. MATHERON 's & J. SERRA 's schools.     

Invited review: Aging and sarcopenia.

Aging is associated with progressive loss of neuromuscular function that often leads to progressive disability and loss of independence. The term sarcopenia is now commonly used to describe the loss of skeletal muscle mass and strength that occurs in concert with biological aging. By the seventh and eighth decade of life, maximal voluntary contractile strength is decreased, on average, by 20-40% for both men and women in proximal and distal muscles. Although age-associated decreases in strength per unit muscle mass, or muscle quality, may play a role, the majority of strength loss can be accounted for by decreased muscle mass. Multiple factors lead to the development of sarcopenia and the associated impact on function. Loss of skeletal muscle fibers secondary to decreased numbers of motoneurons appears to be a major contributing influence, but other factors, including decreased physical activity, altered hormonal status, decreased total caloric and protein intake, inflammatory mediators, and factors leading to altered protein synthesis, must also be considered. The prevalence of sarcopenia, which may be as high as 30% for those >/=60 yr, will increase as the percentage of the very old continues to grow in our populations. The link between sarcopenia and disability among elderly men and women highlights the need for continued research into the development of the most effective interventions to prevent or at least partially reverse sarcopenia, including the role of resistance exercise and other novel pharmacological and nutritional interventions.     

Multiple mating and reproductive skew in Trinidadian guppies

Male offspring production in promiscuously mating species is typically more skewed than female offspring production. It is therefore advantageous for males to seek as many mating partners as possible. However, given the documented benefits of polyandry we expect females, as well as males, to mate multiply. We tested these ideas using Trinidadian guppies, Poecilia reticulata. Fishes were collected from the wild, housed in groups of 10 males and 10 females and allowed to reproduce freely over a period of three months. We used hypervariable microsatellite loci to identify the parents of 840 offspring and to quantify the variance in mating success. As anticipated, and in line with the Bateman gradient, there was greater skew in the number of progeny produced by males. By contrast, we found no sex difference in mating partner number over the duration of the experiment. A median of two males fathered each brood and there was marked turnover in the identities of the sires of successive broods. Female partner turnover was, however, less than expected under random mating. We suggest that partner switching over time, as well as polyandry within broods, could contribute to the maintenance of genetic diversity in guppy populations.     

Invited review: Theories of aging.

Several factors (the lengthening of the average and, to a lesser extent, of the maximum human life span; the increase in percentage of elderly in the population and in the proportion of the national expenditure utilized by the elderly) have stimulated and continue to expand the study of aging. Recently, the view of aging as an extremely complex multifactorial process has replaced the earlier search for a distinct cause such as a single gene or the decline of a key body system. This minireview keeps in mind the multiplicity of mechanisms regulating aging; examines them at the molecular, cellular, and systemic levels; and explores the possibility of interactions at these three levels. The heterogeneity of the aging phenotype among individuals of the same species and differences in longevity among species underline the contribution of both genetic and environmental factors in shaping the life span. Thus, the presence of several trajectories of the life span, from incidence of disease and disability to absence of pathology and persistence of function, suggest that it is possible to experimentally (e.g., by calorie restriction) prolong functional plasticity and life span. In this minireview, several theories are identified only briefly; a few (evolutionary, gene regulation, cellular senescence, free radical, and neuro-endocrineimmuno theories) are discussed in more detail, at molecular, cellular, and systemic levels.     

Invited review: Aging and energy balance.

Humans over 70 yr of age often lose weight. This appears to be due to a physiological anorexia of aging as well as a loss of lean mass (sarcopenia) and, to a lesser extent, fat mass. The causes of the physiological anorexia of aging include changes in taste and smell and a decrease in adaptive relaxation of the fundus of the stomach, which leads to more rapid antral filling and early satiation. In addition, basal and stimulated levels of the satiating hormone, cholecystokinin, are increased. In men, the decline in testosterone leads to an increase in leptin and a loss of lean mass. Although resting metabolic rate declines with aging, this is mainly due to the decline in lean body mass. Energy metabolism is also decreased due to a decline in Na+-K+-ATPase activity, decreased muscle protein turnover, and possibly changes in mitochondrial membrane protein permeability. Physical energy expenditure declines with aging. Meal-induced thermogenesis shows a delay to peak, possibly due to a delay in gastric emptying. Inadequate data are available on the effect of aging in humans on other energy-producing mechanisms such as adaptive thermogenesis. These physiological changes place older men and women at major risk of developing pathological weight loss when they develop disease states, especially those associated with cytokine elaboration.     

Inbreeding avoidance and reproductive skew in a cooperative mammal

In animal social groups, socially subordinate individuals frequently show low reproductive success or completely fail to breed. This suppression of subordinate reproduction is currently typically attributed to control by dominant individuals. However, subordinates in cooperative groups often lack access to unrelated mates, and an alternative possibility is that their reproduction is limited by inbreeding avoidance. Using the eusocial Damaraland mole-rat Cryptomys damarensis, this paper provides the first experimental evidence, to our knowledge, for this explanation. Subordinate, non-breeding female mole-rats were given access to unrelated mates while remaining in the presence of dominant females, and many became reproductively active soon after unrelated males were introduced. Inbreeding avoidance and the availability of unrelated mates provides a plausible and untested explanation for variation in reproductive skew across animal societies.     

Female dominance status and fecal corticoids in a cooperative breeder with low reproductive skew: ring-tailed lemurs (Lemur catta)

Many studies have shown that low dominance status within a social group is associated with elevated glucocorticoid hormone production, a common index of physiological stress. However, the reverse may be true among cooperatively breeding female mammals with high reproductive skew; that is, high dominance status is associated with elevated glucocorticoid levels. Elevated glucocorticoid levels in these dominant females may be a product of their being the only breeder within a group or may result from other challenges associated with high status. To test this difference, we studied fecal corticoid levels in cooperative breeding females with low reproductive skew (i.e., where reproduction is not limited to dominant group members): ring-tailed lemurs (Lemur catta). We collected behavioral and fecal corticoid data from 39 ring-tailed lemur females from eight groups across three sites. In seven of the eight groups, either one or both of the two most dominant females (ranks 1 and 2) exhibited the highest fecal corticoid levels in the groups. The best predictor of corticoid levels in high-ranking females was the proportion of aggressive agonistic interactions they initiated. For the lower-ranking females the best predictors of elevated corticoid levels were being the recipient of aggressive attacks and being relatively close to one's nearest neighbors. These results differ from many studies of caged male mammals where subordinate individuals often exhibit the highest glucocorticoid levels of a group. Furthermore, the results indicate that reproduction itself is not the primary reason for higher glucocorticoid levels among dominant cooperative-breeding females, but that some other factor must account for these elevated levels.     

Invited review: the mitochondrion in osteoarthritis

In a variety of tissues, cumulative oxidative stress, disrupted mitochondrial respiration, and mitochondrial damage promote aging, cell death, and ultimately, functional failure and degeneration. Because articular cartilage chondroyctes are highly glycolytic, mitochondrially mediated pathogenesis has not been previously applied in models for pathogenesis of osteoarthritis (OA), a cartilage degenerative disease that increases markedly in aging. However, chondrocyte mitochondria respire in vitro and they demonstrate swelling and changes in number in situ in the course of OA. Normal chondrocyte mitochondrial function is hypothesized to critically support adenosine triphosphate (ATP) reserves in functional stressed chondrocytes during OA evolution. In this model, disruption of chondrocyte respiration by nitric oxide, a mediator markedly up-regulated in OA cartilage, is centrally involved in chondrocyte functional compromise. Furthermore, mitochondrial dysfunction can mediate several specific pathogenic pathways implicated in OA. These include oxidative stress, inadequacy of chondrocyte biosynthetic and growth responses, up-regulated chondrocyte cytokine-induced inflammation and matrix catabolism, increased chondrocyte apoptosis, and pathologic cartilage matrix calcification. In addition, the direct, sublethal impairment of chondrocyte mitochondrial ATP synthesis in vitro decreases matrix synthesis and increases matrix calcification ('disease in a dish'). The weight of evidence reviewed herein strongly supports chondrocyte mitochondrial impairment as a mediator of the establishment and progression of OA.     

Clutch-size adjustments and skew models: effects on reproductive partitioning and group stability

Reproductive skew theory seeks to integrate social and ecologicalfactors thought to influence the division of reproduction amonggroup-living animals. However, most reproductive skew modelsonly examine interactions between individuals of the same sex.Here, we suggest that females can influence group stabilityand conflict among males by modifying their clutch size andmay do so if they benefit from the presence of subordinate malehelpers or from reduced conflict. We develop 3 models, basedon concessions-based, restraint, and tug-of-war models, in whichfemale clutch size is variable and ask when females will increasetheir clutch size above that which would be optimal in the absenceof male–male conflict. In concessions-based and restraintmodels, females should increase clutch size above their optimaif the benefits of staying for subordinate males are relativelylow. Relatedness between males has no effect on clutch size.When females do increase clutch size, the division of reproductionbetween males is not influenced by relatedness and does notdiffer between restraint and concessions-based models. Bothof these predictions are in sharp contrast to previous models.In tug-of-war models, clutch size is strongly influenced byrelatedness between males, with the largest clutches, but thefewest surviving offspring, produced when males are unrelated.These 3 models demonstrate the importance of considering third-partyinterests in the decisions of group-living organisms.     

Sociality, mating system and reproductive skew in marmots: evidence and hypotheses

Marmot species exhibit a great diversity of social structure, mating systems and reproductive skew. In particular, among the social species (i.e. all except Marmota monax), the yellow-bellied marmot appears quite different from the others. The yellow-bellied marmot is primarily polygynous with an intermediate level of sociality and low reproductive skew among females. In contrast, all other social marmot species are mainly monogamous, highly social and with marked reproductive skew among females. To understand the evolution of this difference in reproductive skew, I examined four possible explanations identified from reproductive skew theory. From the literature, I then reviewed evidence to investigate if marmot species differ in: (1) the ability of dominants to control the reproduction of subordinates; (2) the degree of relatedness between group members; (3) the benefit for subordinates of remaining in the social group; and (4) the benefit for dominants of retaining subordinates. I found that the optimal skew hypothesis may apply for both sets of species. I suggest that yellow-bellied marmot females may benefit from retaining subordinate females and in return have to concede them reproduction. On the contrary, monogamous marmot species may gain by suppressing the reproduction of subordinate females to maximise the efficiency of social thermoregulation, even at the risk of departure of subordinate females from the family group. Finally, I discuss scenarios for the simultaneous evolution of sociality, monogamy and reproductive skew in marmots.     

Invited review: genetic dissection of sleep.

Recent advances in genomics open up new avenues in the analysis of complex behaviors such as sleep. In this analysis, the mouse is the model species of choice because it is amenable to high throughput phenotype and genotype analysis. With the use of the mouse model, unprecedented progress in our understanding of sleep physiology and the treatment of sleep disorders is awaited. This review is intended to provide an overview of available methods and techniques for genetic dissection of sleep in mice. Limits and advantages of different approaches are discussed to highlight the necessity for combining methods to avoid erroneous interpretations. The gap between understanding mechanisms of sleep and its functions may be bridged by finding its molecular bases.