Sexually transmitted infections in polygamous mating systems

Sexually transmitted infections (STIs) are often associated with chronic diseases and can have severe impacts on host reproductive success. For airborne or socially transmitted pathogens, patterns of contact by which the infection spreads tend to be dispersed and each contact may be of very short duration. By contrast, the transmission pathways for STIs are usually characterized by repeated contacts with a small subset of the population. Here we review how heterogeneity in sexual contact patterns can influence epidemiological dynamics, and present a simple model of polygyny/polyandry to illustrate the impact of biased mating systems on disease incidence and pathogen virulence.     

Sexually transmitted diseases of insects: distribution, evolution, ecology and host behaviour

Sexually transmitted diseases (STDs) of insects are known from the mites, nematodes, fungi, protists and viruses. In total 73 species of parasite and pathogen from approximately 182 species of host have been reported. Whereas nearly all vertebrate STDs are viruses or bacteria, the majority of insect STDs are multicellular ectoparasites, protistans or fungi. Insect STDs display a range of transmission modes, with 'pure' sexual transmission only described from ectoparasites, all of which are mites, fungi or nematodes, whereas the microparasitic endo-parasites tend to show vertical as well as sexual transmission. The distribution of STDs within taxa of insect hosts appears to be related to the life histories of the hosts. In particular, STDs will not be able to persist if host adult generations do not overlap unless they are also transmitted by some alternative route. This explains the observation that the Coleoptera seem to suffer from more STDs than other insect orders, since they tend to diapause as adults and are therefore more likely to have overlapping generations of adults in temperate regions. STDs of insects are often highly pathogenic, and are frequently responsible for sterilizing their hosts, a feature which is also found in mammalian STDs. This, combined with high prevalences indicates that STDs can be important in the evolution and ecology of their hosts. Although attempts to demonstrate mate choice for uninfected partners have so far failed it is likely that STDs have other effects on host mating behaviour, and there is evidence from a few systems that they might manipulate their hosts to cause them to mate more frequently. STDs may also play a part in sexual conflict, with males in some systems possibly gaining a selective advantage from transmitting certain STDs to females. STDs may well be important factors in host population dynamics, and some have the potential to be useful biological control agents, but empirical studies on these subjects are lacking.     

Sexually transmitted disease and the evolution of mating systems

Sexually transmitted diseases (STDs) have been shown to increase the costs of multiple mating and therefore favor relatively monogamous mating strategies. We examine another way in which STDs can influence mating systems in species in which female choice is important. Because more popular males are more likely to become infected, STDs can counteract any selective pressure that generates strong mating skews. We build two models to investigate female mate choice when the sexual behavior of females determines the prevalence of infection in the population. The first model has no explicit social structure. The second model considers the spatial distribution of matings under social monogamy, when females mated to unattractive males seek extrapair fertilizations from attractive males. In both cases, the STD has the potential to drastically reduce the mating skew. However, this reduction does not always happen. If the per contact transmission probability is low, the disease dies out and is of no consequence. In contrast, if the transmission probability is very high, males are likely to be infected regardless of their attractiveness, and mating with the most attractive males imposes again no extra cost for the female. We also show that optimal female responses to the risk of STDs can buffer the prevalence of infection to remain constant, or even decrease, with increasing per contact transmission probabilities. In all cases considered, the feedback between mate choice strategies and STD prevalence creates frequency-dependent fitness benefits for the two alternative female phenotypes considered (choosy vs. randomly mating females or faithful vs. unfaithful females). This maintains mixed evolutionarily stable strategies or polymorphisms in female behavior. In this way, a sexually transmitted disease can stabilize the populationwide proportion of females that mate with the most attractive males or that seek extrapair copulations.     

Populations and infectious diseases: Dynamics and evolution

The host-parasite or host-pathogen system was analyzed from dynamical and evolutionary viewpoints using simple mathematical models incorporating vertical transmission, immunity and its loss. We first analyzed a model without density regulation of host population. In the analysis on dynamics, the condition for the pathogen to work as a density regulating factor was obtained. In the analysis on evolution, criteria for the evolution of host and pathogen were proposed. These criteria implies that the evolution of hosts should result in an increase in infected host density, whereas the evolution of pathogens a decrease in susceptible host density. The direction of evolution at some parameters of host and that of pathogen were examined when the parameters were independently and freely changeable. Among the parameters, only reduction in additional mortality due to infection was the evolutionary trend common to both host and pathogen. In all the other parameters examined, trend of evolution predicted in host is reversed in pathogen. We then analyzed whether the obtained criteria still hold in models with density regulation of hosts. Using randomly generated parameter sets, we obtained the result that the criteria should hold very likely though they do not always hold. We discussed evolution of virulence when there is a constraint between the traits.     

Complex heterochrony underlies the evolution of Caenorhabditis elegans hermaphrodite sex allocation

Hermaphroditic organisms are key models in sex allocation research, yet the developmental processes by which hermaphrodite sex allocation can evolve remain largely unknown. Here we use experimental evolution of hermaphrodite‐male (androdioecious) Caenorhabditis elegans populations to quantify the developmental changes underlying adaptive shifts in hermaphrodite sex allocation. We show that the experimental evolution of increased early‐life self‐fertility occurred through modification of a suite of developmental traits: increased self‐sperm production, accelerated oogenesis and ovulation, and increased embryo retention. The experimental evolution of increased self‐sperm production delayed entry into oogenesis—as expected, given the sequentially coupled production of self‐spermatogenesis and oogenesis. Surprisingly, however, delayed oogenesis onset did not delay reproductive maturity, nor did it trade‐off with gamete or embryo size. Comparing developmental time dynamics of germline and soma indicates that the evolution of increased sperm production did not delay reproductive maturity due to a globally accelerated larval development during the period of self‐spermatogenesis. Overall, heterochrony in gametogenesis and soma can explain adaptive shifts in hermaphrodite sex allocation.     

The importance of reproductive interference in ecology and evolution: from organisms to communities

Knowledge of species interactions is vital to understand ecological and evolutionary patterns in nature. Traditional species interactions (e.g., competition, predation, symbiosis) have received a great deal of deserved attention and their general importance in shaping the evolution of populations and structure of communities is unquestioned. Recently, reproductive interference has been receiving attention as an important species interaction. Reproductive interference is defined as interspecific reproductive activities that decrease the fitness of at least one of the species involved in the interaction. Reproductive interference has the potential to affect the evolutionary trajectories of populations and structure of communities. Here, I comment on seven papers that make up this special feature on reproductive interference. Along the way I highlight key discoveries of these studies and areas of research that may contribute to our understanding of the causes and consequences of reproductive interference.     

Pathogen survival in the external environment and the evolution of virulence

Recent studies have provided evolutionary explanations for much of the variation in mortality among human infectious diseases. One gap in this knowledge concerns respiratory tract pathogens transmitted from person to person by direct contact or through environmental contamination. The sit-and-wait hypothesis predicts that virulence should be positively correlated with durability in the external environment because high durability reduces the dependence of transmission on host mobility. Reviewing the epidemiological and medical literature, we confirm this prediction for respiratory tract pathogens of humans. Our results clearly distinguish a high-virulence high-survival group of variola (smallpox) virus, Mycobacterium tuberculosis, Cornynebacterium diphtheriae, Bordetella pertussis, Streptococcus pneumoniae, and influenza virus (where all pathogens have a mean percent mortality > or = 0.01% and mean survival time >10 days) from a low-virulence low-survival group containing ten other pathogens. The correlation between virulence and durability explains three to four times of magnitude of difference in mean percent mortality and mean survival time, using both across-species and phylogenetically controlled analyses. Our findings bear on several areas of active research and public health policy: (1) many pathogens used in the biological control of insects are potential sit-and-wait pathogens as they combine three attributes that are advantageous for pest control: high virulence, long durability after application, and host specificity; (2) emerging pathogens such as the 'hospital superbug' methicillin-resistant Staphylococcus aureus (MRSA) and potential bioweapons pathogens such as smallpox virus and anthrax that are particularly dangerous can be discerned by quantifying their durability; (3) hospital settings and the AIDS pandemic may provide footholds for emerging sit-and-wait pathogens; and (4) studies on food-borne and insect pathogens point to future research considering the potential evolutionary trade-offs and genetic linkages between virulence and durability.     

Sperm competition and the evolution of testes size in birds

Comparative analyses suggest that a variety of ecological and behavioural factors contribute to the tremendous variability in extrapair mating among birds. In an analysis of 1010 species of birds, we examined several ecological and behavioural factors in relation to testes size; an index of sperm competition and the extent of extrapair mating. In univariate and multivariate analyses, testes size was significantly larger in species that breed colonially than in species that breed solitarily, suggesting that higher breeding density is associated with greater sperm competition. After controlling for phylogenetic effects and other ecological variables, testes size was also larger in taxa that did not participate in feeding their offspring. In analyses of both the raw species data and phylogenetically independent contrasts, monogamous taxa had smaller testes than taxa with multiple social mates, and testes size tended to increase with clutch size, which suggests that sperm depletion may play a role in the evolution of testes size. Our results suggest that traditional ecological and behavioural variables, such as social mating system, breeding density and male parental care can account for a significant portion of the variation in sperm competition in birds.     

Lifetime monogamy and the evolution of eusociality

All evidence currently available indicates that obligatory sterile eusocial castes only arose via the association of lifetime monogamous parents and offspring. This is consistent with Hamilton''s rule (br_s > r_oc), but implies that relatedness cancels out of the equation because average relatedness to siblings (r_s) and offspring (r_o) are both predictably 0.5. This equality implies that any infinitesimally small benefit of helping at the maternal nest (b), relative to the cost in personal reproduction (c) that persists throughout the lifespan of entire cohorts of helpers suffices to establish permanent eusociality, so that group benefits can increase gradually during, but mostly after the transition. The monogamy window can be conceptualized as a singularity comparable with the single zygote commitment of gametes in eukaryotes. The increase of colony size in ants, bees, wasps and termites is thus analogous to the evolution of multicellularity. Focusing on lifetime monogamy as a universal precondition for the evolution of obligate eusociality simplifies the theory and may help to resolve controversies about levels of selection and targets of adaptation. The monogamy window underlines that cooperative breeding and eusociality are different domains of social evolution, characterized by different sectors of parameter space for Hamilton''s rule.     

Mating games: the evolution of human mating transactions

We propose a new, evolutionary, game-theoretic model of conditionalhuman mating strategies that integrates currently disconnectedbodies of data into a single mathematically-explicit theoryof human mating transactions. The model focuses on the problemof how much resource a male must provide to a female to secureand retain her as a mate. By using bidding-game models, we showhow the male's minimally required resource incentive variesas a function of his own mate value, the value of the female,and the distribution of the mate values of their available alternativemates. The resulting theory parsimoniously accounts for strategicpluralism within the sexes, mate choice differences betweenthe sexes, and assortative mating, while generating a rich setof testable new predictions about human mating behavior.     

The origin and evolution of social life in the Stenogastrinae (Hymenoptera,Vespidae)

The Stenogastrinae are a subfamily of the Vespidae. The main difference between these and other social wasps (Polistinae and Vespinae) is a jelly-like substance that the Stenogastrinae secrete from the Dufour 's gland and use in many functions of their biology. It is suggested that this substance greatly contributed to the evolution of social life in these wasps by making it possible to nourish the brood with liquid food and store it in the nest, thus favoring also the evolution of the behavioral mechanisms which facilitated interactions between adults. Social organization of the colonies may have been kept at a low level through a basic system of continuous temporary helper replacement, while the evolution of large colonies was restrained, as well as by the poor quality of construction material, low egg-laying capacity and limited production of abdominal substance, imperfect social regulatory mechanisms, and the absence of defensive mechanisms of the colonies against large predators.     

High levels of genetic monogamy in the group-living Australian lizard Egernia stokesii

The Australian lizard Egernia stokesii lives in spatially and temporally stable groups of up to 17 individuals. We have recently shown that these groups are comprised of breeding partners, their offspring and, in some cases, highly related adults, providing the first genetic evidence of a family structure in any lizard species. Here we investigated the mating system of E. stokesii using data from up to eight polymorphic microsatellite loci and tested the hypothesis that breeding partners are monogamous both within and between mating seasons. Among 16 laboratory-born litters from field collected gravid females from two sites in South Australia, 75% had a single male parent and no male contributed to more than one litter, indicating a high level of genetic monogamy within a season. Additional analyses of field caught individuals, captured between 1994 and 1998, enabled assignment of parentage for 70 juveniles and subadults. These data showed that most young (88.6%) had both parents from within the same group and that high proportions of males (88.9%) and females (63.6%) have multiple cohorts of offspring only with the same partner. Our results suggest that monogamy both within and between seasons is a common mating strategy of E. stokesii and that breeding partners maintain stable associations together and with multiple cohorts of their offspring over periods of up to at least 5 years.     

Culturally transmitted paternity beliefs and the evolution of human mating behaviour

Recent anthropological findings document how certain lowland South American societies hold beliefs in 'partible paternity', which allow children to have more than one 'biological' father. This contrasts with Western beliefs in 'singular paternity', and biological reality, where children have just one father. Here, mathematical models are used to explore the coevolution of paternity beliefs and the genetic variation underlying human mating behaviour. A gene-culture coevolutionary model found that populations exposed to a range of selection regimes typically converge on one of two simultaneously stable equilibria; one where the population is monogamous and believes in singular paternity, and the other where the population is polygamous and believes in partible paternity. A second agent-based model, with alternative assumptions regarding the formation of mating consortships, broadly replicated this finding in populations with a strongly female-biased sex ratio, consistent with evidence for high adult male mortality in the region. This supports an evolutionary scenario in which ancestral South American populations with differing paternity beliefs were subject to divergent selection on genetically influenced mating behaviour, facilitated by a female-biased sex ratio, leading to the present-day associations of female control, partible paternity and polygamy in some societies, and male control, singular paternity and monogamy in others.     

Correlated paternity measures mate monopolization and scales with the magnitude of sexual selection

Indirect measures of sexual selection have been criticized because they can overestimate the magnitude of selection. In particular, they do not account for the degree to which mating opportunities can be monopolized by individuals of the sex that compete for mates. We introduce a measure of mate monopolization (m) based on the magnitude of correlated paternity and evaluate its ability to track changes in the magnitude of sexual selection. Simulation models were used to compare how well m tracked changes in the selection differential (s) for a trait regulating mating success. We further evaluated the association between m and s using ten replicate mating arrays of Sagittaria latifolia in which plants with contrasting alleles at microsatellite loci competed for siring opportunities. The computer models and mating arrays both demonstrated a positive linear association between m and s, supporting the utility of m as an index of sexual selection. Commonly used measures of sexual selection are not easily applied to organisms, such as the flowering plants, for which mating events are difficult to observe. The measure of mate monopolization introduced here could prove to be a useful addition to studies of sexual selection in these organisms.     

On the Relative Importance of Haplo-Diploidy, Assortative Mating and Social Synergy on the Evolutionary Emergence of Social Behavior

Advances in multiagent simulation techniques make it possible to study more realistic dynamics of complex systems and allow evolutionary theories to be tested. Here I use simulations to assess the relative importance of reproductive systems (haplodiploidy vs. diploidy), mate selection (assortative mating vs. random mating) and social economics (pay-off matrices of evolutionary games) in the evolutionary dynamics leading to the emergence of social cooperation in the provision of parental care. The simulations confirm that haplo-diploid organisms and organisms mating assortatively have a higher probability for fixing alleles and require less favorable conditions for their fixation, than diploids or organisms mating randomly. The simulations showed that social behavior was most likely to emerge a) when the cost for parental investment was much lower than the benefits to the offspring, b) when cooperation improved synergistically the fitness of offspring compared to the corresponding egoistic behavior and c) when alleles coding for altruistic or social behavior could be rapidly fixed in the population, thanks to mechanisms such as haplo-diploidy and/or assortative mating. Cooperative social behavior always appeared if sociality conferred much higher fitness gains compared to non cooperative alternatives suggesting that the most important factors for the emergence and maintenance of social behavior are those based on energetic or efficiency considerations. The simulations, in congruence with the scant experimental evidence available, suggest that economic considerations rather than genetic ones are critical in explaining the emergence and maintenance of sociality.     

Wing serial homologs and the origin and evolution of the insect wing

The origin and evolution of insect wings has been the subject of extensive debate. The issue has remained controversial largely because of the absence of definitive fossil evidence or direct developmental evidence of homology between wings and a putative wing origin. Recent identification of wing serial homologs (WSHs) has provided researchers with a potential strategy for identifying WSHs in other species. Future comparative developmental analyses between wings and WSHs may clarify the important steps underlying the evolution of insect wings.