Life history and mating systems select for male biased parasitism mediated through natural selection and ecological feedbacks

tlsb-1%Males are often the ‘sicker’ sex with male biased parasitism found in a taxonomically diverse range of species. There is considerable interest in the processes that could underlie the evolution of sex-biased parasitism. Mating system differences along with differences in lifespan may play a key role. We examine whether these factors are likely to lead to male-biased parasitism through natural selection taking into account the critical role that ecological feedbacks play in the evolution of defence. We use a host-parasite model with two-sexes and the techniques of adaptive dynamics to investigate how mating system and sexual differences in competitive ability and longevity can select for a bias in the rates of parasitism. Male-biased parasitism is selected for when males have a shorter average lifespan or when males are subject to greater competition for resources. Male-biased parasitism evolves as a consequence of sexual differences in life-history that produce a greater proportion of susceptible females than males and therefore reduce the cost of avoiding parasitism in males. Different mating systems such as monogamy, polygyny or polyandry did not produce a bias in parasitism through these ecological feedbacks but may accentuate an existing bias.     

Determinants of natural mating success in the cannibalistic orb-web spider Argiope bruennichi

Monogynous mating systems (low male mating rates) occur in various taxa and have evolved several times independently in spiders. Monogyny is associated with remarkable male mating strategies and predicted to evolve under a male-biased sex ratio. While male reproductive strategies are well documented and male mating rates are easy to quantify, especially in sexually cannibalistic species, female reproductive strategies, the optimal female mating rate, and the factors that affect the evolution of female mating rates are still unclear. In this study, we examined natural female mating rates and tested the assumption of a male-biased sex ratio and female polyandry in a natural population of Argiope bruennichi in which we controlled female mating status prior to observations. We predicted variation in female mating frequencies as a result of spatial and temporal heterogeneity in the distribution of mature females and males. Females had a low average mating rate of 1.3 and the majority copulated only once. Polyandry did not entirely result from a male-biased sex-ratio but closely matched the rate of male bigamy. Male activity and the probability of polyandry correlated with factors affecting pheromone presence such as virgin females' density. We conclude that a strong sex ratio bias and high female mating rates are not necessary components of monogynous mating systems as long as males protect their paternity effectively and certain frequencies of bigyny stabilise the mating system.     

An excess of males: skewed sex ratios in bat flies (Diptera: Streblidae)

Ectoparasitic insects often exhibit female-biased sex ratios, a pattern usually explained by greater female longevity and the likelihood that smaller, more active males will disperse or be groomed off the host. Theory predicts that unbalanced sex ratios should favor males when resources are abundant and predictable, and when males are the dispersing sex. Sex ratios of streblid bat flies were evaluated based on a large biodiversity survey in Venezuela–more than 25,000 bats representing 130 species were searched for flies, yielding more than 36,500 bat flies of 116 species. These samples allowed us to analyze sex ratios in 112 bat fly metapopulations. Our results indicate that fully one-third of these metapopulations were significantly male-biased. Traditional explanations for sex-ratio bias, such as sampling effects, unequal longevity between the sexes, and differential dispersal capability are refuted for bat flies in favor of an alternative hypothesis—selective host grooming. Because host grooming is the principal cause of mortality for these slow-reproducing parasites, and because females are larger than males and gravid for a significant portion of their adult life, host grooming activity is more likely to kill or remove females than males. Incomplete understanding of population dynamics, such as mating behavior, dispersal, and reproductive success, cloud applications of male-biased sex ratios in bat flies to support or refute theoretical predictions. Population studies of mating competition and sex-related dispersal dynamics of this male-dominated group should yield important insights into sex ratio theory.     

Effects of water mites on the damselfly Ceriagrion tenellum

1. Water mite parasitism is expected to have an important effect on damselfly survivorship and reproductive success, because mites drain considerable amounts of body fluids from their hosts. This study tests the effect of water mite parasitism in a marked population of the damselfly Ceriagrion tenellum during 1995 (individuals marked as mature adults) and 1996 (individuals marked as tenerals).
2. Almost all teneral individuals were parasitized (98%) and mites were aggregated strongly on some individuals. Parasite load increased during the season.
3. Parasites had no effect on the probability of recapture of hosts as mature adults. The average daily survival rate of lightly- and heavily-parasitized individuals, estimated with Jolly's stochastic method, did not differ significantly.
4. In 1995 parasites had a significant effect on host mating success. The probability of mating was about 25% lower for heavily-parasitized males than for lightly-parasitized males. Lightly-parasitized males also mated more times than heavily-parasitized males, even if heavily-parasitized males lived longer. In 1996, parasitism did not have an effect on male mating success. In both years mites had no effect on female lifetime mating success.
5. These results indicate that water mite parasitism does not reduce damselfly survivorship, but it could reduce male mating success in some circumstances. Further long-term studies are needed, especially in populations with a lower incidence of parasitism.     

Costs of aggregation: shadow competition in a sit-and-wait predator

The role of top-down (e.g. parasitism) and bottom-up (e.g. resource competition) processes is of fundamental importance for the stability and persistence of insect herbivore populations. Although emphasis has often focused on single regulatory agents, the processes underpinning tri-trophic interactions may actually be more pluralistic. Recently, further complexities involved in the regulation of tri-trophic systems have been highlighted. In particular, life history characteristics may have a concomitant role when coupled with the regulatory effects of resource competition and/or parasitism. Here we present an age-structured model to investigate the effects of larval development period, parasitism and resource competition on the stability and persistence of herbivore–parasitoid interactions. We show that the influence of weak density dependent parasitism is sufficient to stabilise the interaction when the period of host susceptibility to parasitism is short. For longer periods of host susceptibility, parasitism needs to be highly non-linear to overcome the destabilising effects of the time delays. In systems where host development is protracted through the season we predict that resource competition is likely to be the dominant process for herbivore regulation. We use this age-structured approach to explore the population dynamics of two field studies from temperate ecosystems. Predictions from these case studies show 1) that both the strength and type of competition and parasitism are important for the stability and persistence of the particular system, and 2) that the length of the developmental period of the vulnerable host is critical to understand the influence of different regulatory processes. Host demography is of overriding importance in determining whether herbivores show outbreaks, and which particular ecological processes and mechanisms are responsible for generating such overcompensatory dynamics.     

Sexually transmitted diseases in polygynous mating systems: prevalence and impact on reproductive success

Studies of disease in relation to animal mating systems have focused on sexual selection and the evolution of sexual reproduction. Relatively little work has examined other aspects of ecological and evolutionary relationships between host social and sexual behaviour, and dynamics and prevalence of infectious diseases; this is particularly evident with respect to sexually transmitted diseases (STDs). Here, we use a simulation approach to investigate rates of STD spread in host mating systems ranging from permanent monogamy to serial polygyny or polyandry and complete promiscuity. The model assumes that one sex (female) is differentially attracted to the other, such that groups of varying size are formed within which mating and disease transmission occur. The results show that equilibrium disease levels are generally higher in females than males and are a function of variance in male mating success and the likelihood of a female switching groups between mating seasons. Moreover, initial rates of disease spread (determining whether an STD establishes in a population) depend on patterns of host movement between groups, variance in male mating success and host life history (e.g. mortality rates). Male reproductive success can be reduced substantially by a sterilizing STD and this reduction is greater in males that are more 'attractive' to females. In contrast, females that associate with more attractive males have lower absolute fitness than females associating with less attractive males. Thus, the potential for STDs to act as a constraint on directional selection processes leading to polygyny (or polyandry) is likely to depend on the details of mate choice and group dynamics.     

Do males matter? The role of males in population dynamics

Models of population dynamics generally neglect the presence of males. While this assumption holds under many circumstances, behavioural ecology increasingly tells us that the presence (or absence) of males may have an impact on female fitness, and hence population sizes. Here we ask the question of whether males matter to population dynamics, operationally defined as a dependency of population growth on the relative density of males. We provide simple models, and evaluate the current empirical evidence for them, that illustrate various mechanisms of such male influence: mate searching behavior, male resource use (including effects of sexual dimorphism), sexual harassment and sexual segregation. In each case, theory predicts that males can have an effect on population densities, and in some extreme cases a positive feedback between an increasingly male-biased sex ratio and female harassment may theoretically even bring about population extinction. The results of this study, and the literature reviewed, show that the males can have a substantial effect on population dynamics, particularly so when human influences result in biased sex ratios.     

Polygynous great reed warblers Acrocephalus arundinaceus suffer more cuckoo Cuculus canorus parasitism than monogamous pairs

There is increasing evidence that hosts within a population may not be parasitized by common cuckoos Cuculus canorus with equal probability. Such non‐randomness has been documented, for example, for host nest sites and host quality. In this study we demonstrate association between successful cuckoo parasitism and host social mating system. We found that nests of socially polygynous great reed warblers Acrocephalus arundinaceus were more often successfully parasitized than the nests of their monogamous counterparts. We hypothesize that lack of parental assistance provided by polygynous males to their mates during egg laying period and higher nest activity in their territories could contribute to this discrepancy. These data imply that social mating system should be taken into account in future studies of brood parasitism.     

Behavioral and physiological female responses to male sex ratio bias in a pond-breeding amphibian

Introduction

The phenomenon of sexual conflict has been well documented, and in populations with biased operational sex ratios the consequences for the rarer sex can be severe. Females are typically a limited resource and males often evolve aggressive mating behaviors, which can improve individual fitness for the male while negatively impacting female condition and fitness. In response, females can adjust their behavior to minimize exposure to aggressive mating tactics or minimize the costs of mating harassment. While male-male competition is common in amphibian mating systems, little is known about the consequences or responses of females. The red-spotted newt (Notophthalmus viridescens) is a common pond-breeding amphibian with a complex, well-studied mating system where males aggressively court females. Breeding populations across much of its range have male-biased sex ratios and we predicted that female newts would have behavioral mechanisms to mitigate mating pressure from males. We conducted four experiments examining the costs and behavioral responses of female N. viridescens exposed to a male-biased environment.

Results

In field enclosures, we found that female newts exposed to a male-biased environment during the five-month breeding season ended with lower body condition compared to those in a female-biased environment. Shorter-term exposure to a male-biased environment for five weeks caused a decrease in circulating total leukocyte and lymphocyte abundance in blood, which suggests females experienced physiological stress. In behavioral experiments, we found that females were more agitated in the presence of male chemical cues and females in a male-biased environment spent more time in refuge than those in a female-biased environment.

Conclusions

Our results indicate that male-biased conditions can incur costs to females of decreased condition and potentially increased risk of infection. However, we found that females can also alter their behavior and microhabitat use under a male-biased sex ratio. Consistent with surveys showing reduced detection probabilities for females, our research suggests that females avoid male encounters using edge and substrate habitat. Our work illustrates the integrated suite of impacts that sexual conflict can have on the structure and ecology of a population.     

Conflict over multiple-partner mating between males and females of the polygynandrous common lizards

The optimal number of mate partners for females rarely coincides with that for males, leading to a potential sexual conflict over multiple-partner mating. This suggests that the population sex ratio may affect multiple-partner mating and thus multiple paternity. We investigate the relationship between multiple paternity and the population sex ratio in the polygynandrous common lizard (Lacerta vivipara). In six populations the adult sex ratio was biased toward males, and in another six populations the adult sex ratio was biased toward females, the latter corresponding to the average adult sex ratio encountered in natural populations. In males the frequency and the degree of polygyny were lower in male-biased populations, as expected if competition among males determines polygyny. In females the frequency of polyandry was not different between treatments, and polyandrous females produced larger clutches, suggesting that polyandry might be adaptive. However, in male-biased populations females suffered from reduced reproductive success compared to female-biased populations, and the number of mate partners increased with female body size in polyandrous females. Polyandrous females of male-biased populations showed disproportionately more mating scars, indicating that polyandrous females of male-biased populations had more interactions with males and suggesting that the degree of multiple paternity is controlled by male sexual harassment. Our results thus imply that polyandry may be hierarchically controlled, with females controlling when to mate with multiple partners and male sexual harassment being a proximate determinant of the degree of multiple paternity. The results are also consistent with a sexual conflict in which male behaviors are harmful to females.     

Evolution of dispersal in metacommunities of interacting species

Theoretical studies on the evolution of dispersal in metacommunities are rare despite empirical evidence suggesting that interspecific interactions can modify dispersal behaviour of organisms. To understand the role of species interactions for dispersal evolution, we utilize an individual‐based model of a metacommunity where local population dynamics follows a stochastic version of the Nicholson–Bailey model and dispersal probability is an evolving trait. Our results show that in comparison with a neutral system (commensalism), parasitism promotes dispersal of hosts and parasites, while mutualism tends to reduce dispersal in both partners. Search efficiency of guests (only in the case of parasitism), dispersal mortality and external extinction risk can influence the evolution of dispersal of all partners. In systems composed of two host and two guest species, lower dispersal probabilities evolve under parasitism as well as mutualism than in one host and one guest species systems. This is because of frequency‐dependent modulations of dispersal benefits emerging in such systems for all partners.     

How inbreeding and outbreeding influence the risk of extinction--a genetically explicit model

We have developed a stochastic model to explore the common effect which genetics and demography have on the extinction risk of endangered populations. The dynamics is formulated as a MARKOVian birth and death process (in continuous time), whereby selection acts through different mortalities of each genotype. With the help of this model we are able to show how inbreeding and outbreeding can influence the genetic variability and the survival of a population. Whether inbreeding or outbreeding takes place depends on the specific mating system. In our model we consider positive assortative as well as disassortative mating. In the case of additive fitness we show that inbreeding reduces the extinction risk and the genetic variability.     

Sex ratios and sexual selection in socially monogamous zebra finches

An experiment was performed in which adult sex ratios of zebrafinches, Taeniopygyia guttata castanotis, were varied to testpossible effects of adult population sex ratios on sexual selectionintensity and mating system dynamics in species with biparentalcare. The possibility that sex ratio influences the successof social mating patterns (leading to polygyny when males arerare and polyandry when females are rare) was not supported.Results did support the prediction of the differential allocationhypothesis that individuals of the abundant sex would increasetheir relative parental expenditure (PE). Although total (male+ female) PE did not vary between treatments, relative malePE was significantly higher in the male-biased treatment (MBT;sex ratio 64% male) than in the female-biased treatment (FBT; sexratio 36% male). In both treatments, male PE contributions contributedto female reproductive rate. Results also supported the predictionof the differential access hypothesis that individuals of theabundant sex would experience greater intensity of selectionon sexually selected attributes. Male beak color, a sexuallyselected trait, influenced male social parentage in the MBTbut not in the FBT. Finally, broods in the FBT displayed higher hatchingasynchrony and lower hatching success; we believe this was causedby early onset of incubation, a tactic used as a defense againstintraspecific brood parasitism, which was much higher in theFBT. Population sex ratios may be an important factor affectingfemale ability to influence male parental investment patterns.     

Social organization of the voleClethrionomys rufocanus and its demographic and genetic consequences: A review

Recent findings on the relationship between social interaction and demographic process in the gray-sided voleClethrionomys rufocanus are reviewed with reference to the findings in other microtine rodents. Social behavior was particularly focused on spacing and dispersal, and their effects on population dynamics are discussed. Female territoriality can limit a population abundance as a density-dependent factor, although its regulatory effect is controversial. Female philopatry and male-biased dispersal should bring about the clumped distribution of female relatives and genetically random distribution of males during the breeding season. The sexual difference in dispersal patterns can contribute to the mating behavior of the vole; promiscuous mating and low frequency of incestuous mating. However, effects of social structure, including kinship, on reproduction and survival of individuals still remains to be clarified. Molecular markers may help to solve these issues and provide new field of population ecology in microtine rodents.     

Does Sex-Selective Predation Stabilize or Destabilize Predator-Prey Dynamics?

Background

Little is known about the impact of prey sexual dimorphism on predator-prey dynamics and the impact of sex-selective harvesting and trophy hunting on long-term stability of exploited populations.

Methodology and Principal Findings

We review the quantitative evidence for sex-selective predation and study its long-term consequences using several simple predator-prey models. These models can be also interpreted in terms of feedback between harvesting effort and population size of the harvested species under open-access exploitation. Among the 81 predator-prey pairs found in the literature, male bias in predation is 2.3 times as common as female bias. We show that long-term effects of sex-selective predation depend on the interplay of predation bias and prey mating system. Predation on the ‘less limiting’ prey sex can yield a stable predator-prey equilibrium, while predation on the other sex usually destabilizes the dynamics and promotes population collapses. For prey mating systems that we consider, males are less limiting except for polyandry and polyandrogyny, and male-biased predation alone on such prey can stabilize otherwise unstable dynamics. On the contrary, our results suggest that female-biased predation on polygynous, polygynandrous or monogamous prey requires other stabilizing mechanisms to persist.

Conclusions and Significance

Our modelling results suggest that the observed skew towards male-biased predation might reflect, in addition to sexual selection, the evolutionary history of predator-prey interactions. More focus on these phenomena can yield additional and interesting insights as to which mechanisms maintain the persistence of predator-prey pairs over ecological and evolutionary timescales. Our results can also have implications for long-term sustainability of harvesting and trophy hunting of sexually dimorphic species.     

Modelling the Evolution of Traits in a Two-Sex Population,with an Application to Grandmothering

We present a mathematical simplification for the evolutionary dynamics of a heritable trait within a two-sex population. This trait is assumed to control the timing of sex-specific life-history events, such as the age of sexual maturity and end of female fertility, and each sex has a distinct fitness trade-off associated with the trait. We provide a formula for the fitness landscape of the population and show a natural extension of the result to an arbitrary number of heritable traits. Our method can be viewed as a dynamical systems generalisation of the Price equation to include two sexes, age structure and multiple traits. We use this formula to examine the effect of grandmothering, whereby post-fertile females subsidise their daughter’s fertility by provisioning grandchildren. Grandmothering can drive a shift towards increasingly male-biased mating sex ratios due to a post-fertile life stage in females, while male fertility continues to older ages. Our fitness landscapes show a net increase in fitness for both males and females at longer lifespans, and as a result, we find that grandmothering alone provides an evolutionary trajectory to higher longevities.     

Directional changes in sexual size dimorphism in shorebirds, gulls and alcids

The Charadrii (shorebirds, gulls and alcids) are one of the most diverse avian groups from the point of view of sexual size dimorphism, exhibiting extremes in both male-biased and female-biased dimorphism, as well as monomorphism. In this study we use phylogenetic comparative analyses to investigate how size dimorphism has changed over evolutionary time, distinguishing between changes that have occurred in females and in males. Independent contrasts analyses show that both body mass and wing length have been more variable in males than in females. Directional analyses show that male-biased dimorphism has increased after inferred transitions towards more polygynous mating systems. There have been analogous increases in female-biased dimorphism after transitions towards more socially polyandrous mating systems. Changes in dimorphism in both directions are attributable to male body size changing more than female body size. We suggest that this might be because females are under stronger natural selection constraints related to fecundity. Taken together, our results suggest that the observed variation in dimorphism of Charadrii can be best explained by male body size responding more sensitively to variable sexual selection than female body size.     

Paternity-parasitism trade-offs: a model and test of host-parasite cooperation in an avian conspecific brood parasite

Efforts to evaluate the evolutionary and ecological dynamics of conspecific brood parasitism in birds and other animals have focused on the fitness costs of parasitism to hosts and fitness benefits to parasites. However, it has been speculated recently that, in species with biparental care, host males might cooperate with parasitic females by allowing access to the host nest in exchange for copulations. We develop a cost-benefit model to explore the conditions under which such host-parasite cooperation might occur. When the brood parasite does not have a nest of her own, the only benefit to the host male is siring some of the parasitic eggs (quasi-parasitism). Cooperation with the parasite is favored when the ratio of host male paternity of his own eggs relative to his paternity of parasitic eggs exceeds the cost of parasitism. When the brood parasite has a nest of her own, a host male can gain additional, potentially more important benefits by siring the high-value, low-cost eggs laid by the parasite in her own nest. Under these conditions, host males should be even more likely to accept parasitic eggs in return for copulations with the parasitic female. We tested these predictions for American coots (Fulica americana), a species with a high frequency of conspecific brood parasitism. Multilocus DNA profiling indicated that host males did not sire any of the parasitic eggs laid in host nests, nor did they sire eggs laid by the parasite in her own nest. We used field estimates of the model parameters from a four-year study of coots to predict the minimum levels of paternity required for the costs of parasitism to be offset by the benefits of mating with brood parasites. Observed levels of paternity were significantly lower than those predicted under a variety of assumptions, and we reject the hypothesis that host males cooperated with parasitic females. Our model clarifies the specific costs and benefits that influence host-parasite cooperation and, more generally, yields precise predictions about expected levels of host male paternity. These predictions will enable a more rigorous assessment of field studies designed to test adaptive hypotheses of host-parasite cooperation.     

Effect of mating combinations on the host parasitisation and sex allocation in solitary endoparasitoid,Aenasius arizonensis (Hymenoptera: Encyrtidae)

Aenasius arizonensis (Girault) is an important solitary endoparasitoid of Phenacoccus solenopsis Tinsley. To optimise the mass production of high-quality females, it is important to assess the influence of mating regimes on the progeny fitness and sex allocation. We, therefore, hypothesise that mating combinations in A. arizonensis adults emerged from different host instars may influence parasitism and sex allocation in the subsequent generation. Therefore, we compared three nymphal instars (1st, 2nd and 3rd) and adults host stages of P. solenopsis for parasitism and sex allocation by A. arizonensis. Further, F₁ female progeny of the parasitoid emerged from different host instars was henceforth evaluated for its fitness in six mating combinations. A. arizonensis females parasitised all the host stages except the 1st instar nymphs. The parasitised 2nd instar nymphs yielded only males, while the sex ratio in the later host instars was strongly female-biased. The parasitoid females preferred 3rd instar nymphs with respect to higher parasitism (74.0–84.0%) and produced more females in the F₁ progeny as compared to other host stages. F₁ females that emerged from 3rd instar nymphs produced significantly higher parasitism (74.0–79.0%). These mating combinations also yielded more female progeny in the F₂ generation. However, parasitism by F₁ females was significantly lower (9.0–12.0%) when mated with males that emerged from 2nd instar P. solenopsis nymphs. Moreover, latter combinations yielded only male progeny in F₂ generation. These findings can be used in laboratory mass rearing of this parasitoid vis-à-vis biological control of P. solenopsis.     

Sexual selection, sexual size dimorphism and Rensch's rule in Odonata

Odonata (dragonflies and damselflies) exhibit a range of sexual size dimorphism (SSD) that includes species with male-biased (males > females) or female-biased SSD (males < females) and species exhibiting nonterritorial or territorial mating strategies. Here, we use phylogenetic comparative analyses to investigate the influence of sexual selection on SSD in both suborders: dragonflies (Anisoptera) and damselflies (Zygoptera). First, we show that damselflies have male-biased SSD, and exhibit an allometric relationship between body size and SSD, that is consistent with Rensch's rule. Second, SSD of dragonflies is not different from unit, and this suborder does not exhibit Rensch's rule. Third, we test the influence of sexual selection on SSD using proxy variables of territorial mating strategy and male agility. Using generalized least squares to account for phylogenetic relationships between species, we show that male-biased SSD increases with territoriality in damselflies, but not in dragonflies. Finally, we show that nonagile territorial odonates exhibit male-biased SSD, whereas male agility is not related to SSD in nonterritorial odonates. These results suggest that sexual selection acting on male sizes influences SSD in Odonata. Taken together, our results, along with avian studies (bustards and shorebirds), suggest that male agility influences SSD, although this influence is modulated by territorial mating strategy and thus the likely advantage of being large. Other evolutionary processes, such as fecundity selection and viability selection, however, need further investigation.