Character displacement as the "best of a bad situation": fitness trade-offs resulting from selection to minimize resource and mate competition

Abstract Character displacement has long been considered a major cause of adaptive diversification. When species compete for resources or mates, character displacement minimizes competition by promoting divergence in phenotypes associated with resource use (ecological character displacement) or mate attraction (reproductive character displacement). In this study, we investigated whether character displacement can also have pleiotropic effects that lead to fitness trade-offs between the benefits of avoiding competition and costs accrued in other fitness components. We show that both reproductive and ecological character displacement have caused spadefoot toads to evolve smaller body size in the presence of a heterospecific competitor. Although this shift in size likely arose as a by-product of character displacement acting to promote divergence between species in mating behavior and larval development, it concomitantly reduces offspring survival, female fecundity, and sexual selection on males. Thus, character displacement may represent the "best of a bad situation" in that it lessens competition, but at a cost. Individuals in sympatry with the displaced phenotype will have higher fitness than those without the displaced trait because they experience reduced competition, but they may have reduced fitness relative to individuals in allopatry. Such a fitness trade-off can limit the conditions under which character displacement evolves and may even increase the risk of "Darwinian extinction" in sympatric populations. Consequently, character displacement may not always promote diversification in the manner that is often expected.     

Evolution of reproductive effort in viscous populations: the importance of population dynamics

I present two ecological models for the evolution of reproductive effort in viscous populations with empty sites. In contrast with previous studies, I show that limited dispersal needs not have a positive effect on the evolutionarily stable allocation of resources to fecundity versus survival. Rather, depending on the feedback between the trait and the population dynamics, population viscosity may have no effect or even lead to a decrease in the evolutionarily stable reproductive effort when individuals can degrade their environment during their lifetime. I show that the different evolutionary outcomes can be explained by the asymmetry in the level of kin competition resulting from investing into juveniles or into adults.     

Female Reproductive Fitness Declines with Increasing Male Density in the Polyandrous Weevil Sitophilus oryzae

The effect of male density on female reproductive fitness is still poorly understood in many insect species. Here we examined how male density influenced female mating behaviour, fecundity, longevity and damage to the genital tract in Sitophilus oryzae (L.) (Coleoptera: Curculionidae), an important pest of whole grains worldwide. We show that with increasing male density, (1) both male mate competition and female copulation duration significantly increased and (2) female fecundity, longevity and feeding time significantly decreased. Dissection indicates that the backward pointing spines on the reversed internal sac of male genitalia may grip and damage the female genital tracts. These results suggest that longer copulation and more frequent matings under higher male densities reduce the time for feeding and oviposition and increase the damage to female genital tracts. We conclude that the decreased female reproductive fitness under high male densities is most likely caused by a combination of the decreased feeding and oviposition time and increased damage to female genital tracts.     

Inclusive fitness effects can select for cancer suppression into old age

Natural selection can favour health at youth or middle age (high reproductive value) over health at old age (low reproductive value). This means, all else being equal, selection for cancer suppression should dramatically drop after reproductive age. However, in species with significant parental investment, the capacity to enhance inclusive fitness may increase the reproductive value of older individuals or even those past reproductive age. Variation in parental investment levels could therefore contribute to variation in cancer susceptibility across species. In this article, we describe a simple model and framework for the evolution of cancer suppression with varying levels of parental investment and use this model to make testable predictions about variation in cancer suppression across species. This model can be extended to show that selection for cancer suppression is stronger in species with cooperative breeding systems and intergenerational transfers. We consider three cases that can select for cancer suppression into old age: (i) extended parental care that increases the survivorship of their offspring, (ii) grandparents contributing to higher fecundity of their children and (iii) cooperative breeding where helpers forgo reproduction or even survivorship to assist parents in having higher fecundity.     

Inclusive-fitness logic of cooperative breeding with benefits of natal philopatry

In cooperatively breeding species, individuals help to raise offspring that are not their own. We use two inclusive-fitness models to study the advantage of this kind of helpful behaviour in social groups with high reproductive skew. Our first model does not allow for competition among relatives to occur but our second model does. Specifically, our second model assumes a competitive hierarchy among nest-mates, with non-breeding helpers ranked higher than their newborn siblings. For each model, we obtain an expression for the change in inclusive fitness experienced by a helpful individual in a selfish population. The prediction suggested by each expression is confirmed with computer simulation. When model predictions are compared to one another, we find that helping emerges under a broader range of conditions in the second model. Although competition among kin occurs in our second model, we conclude that the life-history features associated with this competition also act to promote the evolutionary transition from solitary to cooperative breeding.     

Infection of the fittest: devil facial tumour disease has greatest effect on individuals with highest reproductive output

Emerging infectious diseases rarely affect all members of a population equally and determining how individuals’ susceptibility to infection is related to other components of their fitness is critical to understanding disease impacts at a population level and for predicting evolutionary trajectories. We introduce a novel state‐space model framework to investigate survival and fecundity of Tasmanian devils (Sarcophilus harrisii) affected by a transmissible cancer, devil facial tumour disease. We show that those devils that become host to tumours have otherwise greater fitness, with higher survival and fecundity rates prior to disease‐induced death than non‐host individuals that do not become infected, although high tumour loads lead to high mortality. Our finding that individuals with the greatest reproductive value are those most affected by the cancer demonstrates the need to quantify both survival and fecundity in context of disease progression for understanding the impact of disease on wildlife populations.     

Proximate mechanisms of the differences in reproductive success of males bearing different alleles of Pgdh – a gene involved in a sexual conflict in bulb mite

Enzyme polymorphism in phosphogluconate dehydrogenase (Pgdh) is a striking example of single gene polymorphism involved in sexual conflict in bulb mite Rhizoglyphus robini. Males homozygous for the S Pgdh allele were shown to achieve higher reproductive success than FF homozygous males, while negatively influencing fecundity of their female partners. Here, we investigate proximate mechanisms responsible for the increased reproductive success of SS males and find that the S allele is associated with shorter time until copulation, higher copulation frequency and increased sperm production. We also show that Pgdh alleles are probably codominant, with SS males gaining the highest reproductive success, FF males – the lowest – and FS‐heterozygous males taking an intermediate position in all fitness parameters differentiating males of different genotypes. Additionally, we confirm the negative effect that S‐bearing males impose on the fecundity of females they mate with, showing a clear pattern of interlocus sexual conflict. We discuss that this effect is probably associated with increased copulation frequency. Whereas, contrary to what we have predicted, the S allele does not cause increased general male mobility, we speculate that the S allele‐bearing males are more efficient in forcing copulation and/or detecting females.     

Kin selection in age-structured populations

There have been several discussions in the literature as to how to weight interactions between individuals of different ages in models of kin selection. It has commonly been assumed that the reproductive value of a given age is the most appropriate weight, for the purpose of calculating its contribution to inclusive fitness. This paper analyses a model of kin selection in an age-structured population. It is shown that reproductive value is relevant to behavioural interactions involving effects on survival, although the reproductive value of a given age does not provide an exact weighting of its fitness contribution in either discrete- or continuous-time populations. Reproductive value is not relevant to interactions involving effects on fecundity. The results are discussed in relation to observations on behavioural asymmetries involving age differences.     

The influence of male ejaculate quantity on female fitness: a meta‐analysis

Although the primary function of mating is gamete transfer, male ejaculates contain numerous other substances that are produced by accessory glands and transferred to females during mating. Studies with several model organisms have shown that these substances can exert diverse behavioural and physiological effects on females, including altered longevity and reproductive output, yet a comprehensive synthesis across taxa is lacking. Here we use a meta‐analytic approach to synthesize quantitatively extensive experimental work examining how male ejaculate quantity affects different components of female fitness. We summarize effect sizes for female fecundity (partial and lifetime) and longevity from 84 studies conducted on 70 arthropod species that yielded a total of 130 comparisons of female fecundity and 61 comparisons of female longevity. In response to greater amounts of ejaculate, arthropod females demonstrate enhanced fecundity (both partial and lifetime) but reduced longevity, particularly for Diptera and Lepidoptera. Across taxa, multiply mated females show particularly large fecundity increases compared to singly mated females, indicating that single matings do not maximize female fitness. This fecundity increase is balanced by a slight negative effect on lifespan, with females that received more ejaculate through polyandrous matings showing greater reductions in lifespan compared with females that have mated repeatedly with the same male. We found no significant effect size differences for either female fecundity or longevity between taxa that transfer sperm packaged into spermatophores compared to taxa that transfer ejaculates containing free sperm. Furthermore, females that received relatively larger or more spermatophores demonstrated greater lifetime fecundity, indicating that these seminal nuptial gifts provide females with a net fitness benefit. These results contribute to our understanding of the evolutionary origin and maintenance of non‐sperm ejaculate components, and provide insight into female mate choice and optimal mating patterns.     

Path analysis of natural selection via survival and fecundity across contrasting environments in Avena barbata

We employed path analysis to analyse natural selection through two major fitness components in each of three contrasting environments. Using a randomized block design, 188 Recombinant Inbred Lines (RILs) derived from a cross between contrasting ecotypes of Avena barbata were planted in common gardens in the greenhouse, and in two field sites typical of each ecotype’s native habitat. Individuals were monitored for germination phenology, early growth, survival, final size, flowering phenology, reproductive allocation, fecundity and lifetime reproductive success. The variance/covariance matrix of the RIL (genotype) means was fit to a path model in which total fitness was made up of survival and fecundity (of survivors) components. In the greenhouse, all fitness variation was determined by fecundity variation (with no mortality), which was itself primarily determined by reproductive allocation mediated by date of first flowering. By contrast, in the field, early growth was the major determinant of survival, and final size was the major determinant of fecundity. Both components of fitness affected lifetime reproductive success equally in the field. Thus the major difference between greenhouse and field seems to be a shift from selection on allocation patterns in adults, to selection on resource acquisition, especially at earlier life stages. The pattern of selection was similar in the two field sites, despite the contrasting environments.     

Animal dispersal dynamics promoting dioecy over hermaphroditism

Because of the separation of sexual function to male and female individuals, dioecious species have fewer pollen and seed bearers and thus experience disadvantages due to increased aggregation of reproductive function. Because of this disadvantage, models predict that dioecious females must have substantially more than twice the fecundity of hermaphrodites, yet empirical data suggest that female fecundity advantages are commonly much lower. Here, we incorporate animal foraging dynamics--and the heightened dispersal of seeds that may accompany increases in fecundity of dioecious females--into a spatially explicit mathematical model. We focus on the competition for germination sites with varying seed production, seed dispersal ability, and mortality, and we find that preferential foraging on dioecious females reduces the stringent fecundity requirements of dioecy to values in accordance with empirical estimates. This finding contributes to our understanding of the correlation between dioecy and fleshy fruits and highlights the importance of mutualist dispersers to dioecious species.     

Physiological dynamics,reproduction‐maintenance allocations,and life history evolution

Allocation of resources to competing processes of growth, maintenance, or reproduction is arguably a key process driving the physiology of life history trade‐offs and has been shown to affect immune defenses, the evolution of aging, and the evolutionary ecology of offspring quality. Here, we develop a framework to investigate the evolutionary consequences of physiological dynamics by developing theory linking reproductive cell dynamics and components of fitness associated with costly resource allocation decisions to broader life history consequences. We scale these reproductive cell allocation decisions to population‐level survival and fecundity using a life history approach and explore the effects of investment in reproduction or tissue‐specific repair (somatic or reproductive) on the force of selection, reproductive effort, and resource allocation decisions. At the cellular level, we show that investment in protecting reproductive cells increases fitness when reproductive cell maturation rate is high or reproductive cell death is high. At the population level, life history fitness measures show that cellular protection increases reproductive value by differential investment in somatic or reproductive cells and the optimal allocation of resources to reproduction is moulded by this level of investment. Our model provides a framework to understand the evolutionary consequences of physiological processes underlying trade‐offs and highlights the insights to be gained from considering fitness at multiple levels, from cell dynamics through to population growth.     

Socially mediated speciation

Abstract.— We employ a simple model to show that social selection can lead to prezygotic reproductive isolation. The evolution of social discrimination causes the congealing of phenotypically similar individuals into different, spatially distinct tribes. However, tribal formation is only obtained for certain types of social behavior: altruistic and selfish acts can produce tribes, whereas spiteful and mutualistic behaviors never do. Moreover, reduced hybrid fitness at tribal borders leads to the selection of mating preferences, which then spread to the core areas of the respective tribes. Unlike models of resource competition, our model generates reproductive isolation in an ecologically homogeneous environment. We elaborate on how altruistic acts can lead to reproductive isolation, but also predict that certain types of competition can lead to the speciation effect. Our theory provides a framework for how individual-level interactions mold lineage diversification, with parapatric speciation as a possible end product.     

Effect of Body Weight on Reproductive Performance in Cnephasia jactatana (Lepidoptera: Tortricidae)

The larger-the-better theory predicts that fitness is positively linearly associated with body size or weight. We used the kiwifruit pest, Cnephasia jactatana Walker, to test whether larger insects perform better reproductively. We divided our insect population into three weight groups: light, average, and heavy, and assessed the reproductive performance of 9 breeding treatments (3 male weights × 3 female weights). Female fecundity is positively correlated with female body weight in low and average weight groups. There is no such correlation in the heavy weight group, suggesting that further weight increase has no fitness gain for females. The positive linear relationship between fertility and female weight in all weight groups may be attributed to the fact that permanently paired heavy females are more likely to remate, gaining more sperm and thus higher fertility. However, the previous study also indicates that mated females are less likely to be mated again when males have a choice. Therefore, in the natural environment the realized fertility may still follow an asymptotical pattern similar to the fecundity in relation to female weight. Males' beneficial effect on female reproductive outputs increases linearly with their body weight in all weight groups, indicating that male reproductive performance fits the larger-the-better theory. Fertility rate is not affected by the body weight of either sex. Heavy and average females lay eggs earlier and have higher daily fecundity and fertility than light females. Females of all weight groups have similar oviposition and postoviposition periods. Male weight and female–male weight interactions have no effect on oviposition parameters.     

Impaired sperm quality,delayed mating but no costs for offspring fitness in crickets winning a fight

The outcome of male–male contest competition is known to affect male mating success and is believed to confer fitness benefits to females through preference for dominant males. However, by mating with contest winners, females can incur significant costs spanning from decreased fecundity to negative effects on offspring. Hence, identifying costs and benefits of male dominance on female fitness is crucial to unravel the potential for a conflict of interests between the sexes. Here, we investigated males' pre‐ and post‐copulatory reproductive investment and its effect on female fitness after a single contest a using the field cricket Gryllus bimaculatus. We allowed males to fight and immediately measured their mating behaviour, sperm quality and offspring viability. We found that males experiencing a fight, independently of the outcome, delayed matings, but their courtship effort was not affected. However, winners produced sperm of lower quality (viability) compared to losers and to males that did not experience fighting. Results suggest a trade‐off in resource allocation between pre‐ and post‐mating episodes of sexual selection. Despite lower ejaculate quality, we found no fitness costs (fecundity and viability of offspring) for females mated to winners. Overall, our findings highlight the importance of considering fighting ability when assessing male reproductive success, as winners may be impaired in their competitiveness at a post‐mating level.     

Infections with immunogenic trypanosomes reduce tsetse reproductive fitness: potential impact of different parasite strains on vector population structure

The parasite Trypanosoma brucei rhodesiense and its insect vector Glossina morsitans morsitans were used to evaluate the effect of parasite clearance (resistance) as well as the cost of midgut infections on tsetse host fitness. Tsetse flies are viviparous and have a low reproductive capacity, giving birth to only 6-8 progeny during their lifetime. Thus, small perturbations to their reproductive fitness can have a major impact on population densities. We measured the fecundity (number of larval progeny deposited) and mortality in parasite-resistant tsetse females and untreated controls and found no differences. There was, however, a typanosome-specific impact on midgut infections. Infections with an immunogenic parasite line that resulted in prolonged activation of the tsetse immune system delayed intrauterine larval development resulting in the production of fewer progeny over the fly's lifetime. In contrast, parasitism with a second line that failed to activate the immune system did not impose a fecundity cost. Coinfections favored the establishment of the immunogenic parasites in the midgut. We show that a decrease in the synthesis of Glossina Milk gland protein (GmmMgp), a major female accessory gland protein associated with larvagenesis, likely contributed to the reproductive lag observed in infected flies. Mathematical analysis of our empirical results indicated that infection with the immunogenic trypanosomes reduced tsetse fecundity by 30% relative to infections with the non-immunogenic strain. We estimate that a moderate infection prevalence of about 26% with immunogenic parasites has the potential to reduce tsetse populations. Potential repercussions for vector population growth, parasite-host coevolution, and disease prevalence are discussed.     

The Effect of Female Quality on Male Ejaculatory Expenditure and Reproductive Success in a Praying Mantid

Strategic ejaculation is a behavioural strategy shown by many animals as a response to sperm competition and/or as a potential mechanism of cryptic male choice. Males invest more mating resources when the risk of sperm competition increases or they invest more in high quality females to maximize their reproductive output. We tested this hypothesis in the false garden mantid Pseudomantis albofimbriata, where females are capable of multiply mating and body condition is an indicator of potential reproductive fitness. We predicted male mantids would ejaculate strategically by allocating more sperm to high quality females. To determine if and how males alter their ejaculate in response to mate quality, we manipulated female food quantity so that females were either in good condition with many eggs (i.e. high quality) or poor condition with few eggs (i.e. low quality). Half of the females from each treatment were used in mating trials in which transferred sperm was counted before fertilisation occurred and the other half of females were used in mating trials where fertilisation occurred and ootheca mass and total eggs in the ootheca were recorded. Opposed to our predictions, the total number of sperm and the proportion of viable sperm transferred did not vary significantly between female treatments. Male reproductive success was entirely dependent on female quality/fecundity, rather than on the number of sperm transferred. These results suggest that female quality is not a major factor influencing postcopulatory male mating strategies in P. albofimbriata, and that sperm number has little effect on male reproductive success in a single mating scenario.     

Seasonal and lifetime reproductive consequences of inbreeding in the great tit Parus major

Inbreeding depression has been hypothesized to drive the evolutionof mating systems and dispersal. Some studies have shown thatinbreeding strongly affects survival and/or fecundity, but otherstudies suggest that fitness consequences of inbreeding areless detrimental or more complex. We studied consequences ofmating with a relative in a population of great tits (Parusmajor) with a high local recruitment rate. Genotypic informationfrom microsatellite markers was used to calculate coefficientsof kinship, and fitness was measured as seasonal and lifetimereproductive success. We show that mating with a relative affectsseasonal reproductive success, as was found in other studiesof the same species. However, these effects do not result ina lifetime fitness reduction, suggesting that individuals mayhave scope for avoidance of inbreeding after inbreeding depression.Several explanations are proposed as compensatory mechanisms.Although individuals are more likely to divorce after experiencinginbreeding depression, we show that divorce alone cannot explainthe compensation for inbreeding depression in subsequent breedingattempts in our study. We conclude that the costs of matingwith a relative in the short term do not necessarily imply lifetimefitness consequences.     

A new version of the size-advantage hypothesis for sex change: incorporating sperm competition and size-fecundity skew

Traditional sex-change theory cannot explain the existence of protogynous species in which the largest females do not change sex when provided an opportunity. We present an expected reproductive success threshold model that incorporates previously unconsidered factors (size-fecundity skew and sperm competition) that can strongly affect reproductive expectations. The model predicts a variety of circumstances when the largest females remaining in a social group should not change sex in the absence of the dominant male, yet it also predicts that these same conditions should promote sex change in smaller females. If a large female's fecundity is markedly higher than the aggregate of the other members of her social group (i.e., there exists a skew in the size-fecundity distribution that raises a large female's expected reproductive success threshold), she should defer from sex change. Sperm competition can strongly lower the expectation of paternity obtained as a sex-changed male, and this also raises the threshold. The model suggests that deferral of sex change should be more common in species in which intense sperm competition is prevalent (such as fishes living in seagrass beds). This prediction appears consistent with patterns seen in nature.     

Plant performance in central and northern peripheral populations of the widespread Plantago coronopus

Peripheral populations have long been predicted to show lower vital rates, higher demographic fluctuations, and lower densities than central populations. However, recent research has questioned the existence of clear patterns across species’ ranges. To test these hypotheses, we monitored five central and six northern peripheral populations of the widespread herb Plantago coronopus along the European Atlantic coast during 5 yr. We estimated population density, and calculated mean values and temporal variability of four vital rates (survival, individual growth, fecundity and recruitment) in hundreds of plants in permanent plots. Central populations showed higher fecundity, whereas peripheral populations had higher recruitment per reproductive plant, indicating a higher overall reproductive success in the periphery. Central populations showed a marginally significant tendency for higher growth, and there were no differences between range positions in survival. Fecundity and growth were affected by intraspecific competition, and recruitment was affected by precipitation, highlighting the importance of local environmental conditions for population performance. Central and peripheral populations showed no significant differences in temporal variability of vital rates. Finally, density was significantly higher in peripheral than in central populations, in discrepancy with the abundant‐centre model. Density was correlated to seedling recruitment, which would counterbalance in peripheral populations the lower fecundity and the tendency for lower growth of established plants. Such compensations among vital rates might be particularly common in widespread plants, and advise against simplistic assumptions of population performance across ranges. The whole species’ life cycle should be considered, since different arrangements of vital rates are expected to maximize fitness in local environments. Our results show also the importance of discerning between geographical periphery and ecological marginality. In a context of climate‐induced range shifts, these considerations are crucial for the reliability of niche‐models and the management of plant peripheral populations.