Sexual reproduction and diversity: Connection between sexual selection and biological communities via population dynamics

Sexual reproduction is a mysterious phenomenon. Most animals and plants invest in sexual reproduction, even though it is more costly than asexual reproduction. Theoretical studies suggest that occasional or conditional use of sexual reproduction, involving facultative switching between sexual and asexual reproduction, is the optimal reproductive strategy. However, obligate sexual reproduction is common in nature. Recent studies suggest that the evolution of facultative sexual reproduction is prevented by males that coerce females into sexual fertilization; thus, sexual reproduction has the potential to enforce costs on a given species. Here, the effect of sex on biodiversity is explored by evaluating the reproductive costs arising from sex. Sex provides atypical selection pressure that favors traits that increase fertilization success, even at the expense of population growth rates, that is, sexual selection. The strength of sexual selection depends on the density of a given species. Sexual selection often causes strong negative effects on the population growth rates of species that occur at high density. Conversely, a species that reduces its density is released from this negative effect, and so increases its growth rate. Thus, this negative density-dependent effect on population growth that arises from sexual selection could be used to rescue endangered species from extinction, prevent the overgrowth of common species and promote the coexistence of competitive species. Recent publications on sexual reproduction provide several predictions related to the evolution of reproductive strategies, which is an important step toward integrating evolutionary dynamics, demographic dynamics and community dynamics.     

Changes in community size affect the outcome of competition

We examine the role of stochasticity and competitive ability in affecting competition between two species using models derived for population genetics. Just as changing population size affects the fixation of a new mutation, we show that changing the total number of competitors (i.e., community size) can alter the course of competitive exclusion across a wide range of initial starting densities of the two competing species. Shifts in competitive exclusion occur because changes in community size affect the relative importance of competitive ability and stochasticity in affecting the outcome of competition, potentially allowing inferior invaders to usurp superior residents. By shifting the role of stochasticity and competitive ability, any process that changes the total number of competitors in a habitat (e.g., disturbance, eutrophication, fragmentation, predation) may lead to shifts in competitive exclusion and the composition of communities.     

Variation and covariation among life-history traits in Rumex acetosella from a successional old-field gradient

In this study morphological variation and the potential for competition to affect biomass and seedling selection of the families of five populations of Rumex acetosella L. sampled along a successional old-field gradient have been investigated. Seeds from 25 families were submitted to four competitive regimes: no competition (one plant per pot), medium competition (two plants/ pot taking plants from the same population), high within-population competition (four individuals from the same population in a pot) and high between-population competition (four individuals from two different populations in a pot). Eight traits were analysed after 3 months of growth for variation among families within populations. A significant difference among families within the two older populations was recorded for sexual biomass and related components. High sensitivity of these traits to density was observed in all populations except the youngest, suggesting specialization to particular environmental conditions in late successional populations, and a good adaptive capacity to buffer environmental variation in the pioneer population. Little significant interaction between competitive regimes and families within populations was found, i.e. genotypes within each population showed little variation in their response to environmental variation. Genotypic variance decreased with increasing competitive conditions for the majority of the traits. However, the percentage of variance in sexual reproduction explained by family was stable among treatments. Tradeoffs between vegetative reproduction and sexual reproduction were recorded at the population level along the successional gradient, with increasing competitive conditions. As succession proceeds, we observed a decrease in sexual reproduction and an increase in vegetative reproduction. At the family level, correlation among traits were similar when plants were grown in the absence of competition and at high density, with a significant negative correlation between sexual reproduction and vegetative reproduction. For both sprout number and sexual biomass, the performance of families grown under all the treatments was positively correlated. Together these results indicate allocational constraints on the reproductive biology of R. acetosella that may be favoured by natural selection and have influenced population differentiation along the successional gradient. However, they also revealed that the potential exists for evolutionary specialization through plasticity, in response to variation in environmental conditions.     

Variations in sexual and asexual reproduction of Scirpus mariqueter along an elevational gradient

In order to assess the importance of sexual and asexual reproduction during the life history of Scirpus mariqueter, its reproductive and growth characters were concurrently examined along an elevational gradient (from low elevation to high elevation). The proportions of flowering shoot and inflorescence mass, seed : flower ratio and seed weight were used to quantify the investment in sexual reproduction. The proportions of current-year shoot and rhizome mass were used to quantify the investment in asexual reproduction, and the proportion of corm mass was used for growth, respectively. It was found that vegetative propagation predominated at low elevation, whereas sexual reproduction predominated at high elevation; and that sexual reproduction increased with declining asexual reproduction along the gradient. The results suggest that asexual reproduction is relatively favored in the early life stage, whereas sexual reproduction is favored when the population becomes mature and aged, probably because of the functional differentiation between the two reproductive types. Sexual productive characters (i.e. the proportions of flowering shoot and inflorescence mass) were negatively correlated to both growth and asexual reproductive characters along the gradient, indicating there might exist some trade-offs among growth, sexual and asexual reproduction during the life history. However, no obvious pattern was found between asexual reproductive characters and growth characters along the elevational gradient, possibly because of the varied relationships between them at different life stages. The variations in sexual and asexual reproduction in the species and the relationship between them are thought to be of great significance for local population growth, species persistence and evolution.     

Density,parasitism, and sexual reproduction are strongly correlated in lake Daphnia populations

Many organisms can reproduce both asexually and sexually. For cyclical parthenogens, periods of asexual reproduction are punctuated by bouts of sexual reproduction, and the shift from asexual to sexual reproduction has large impacts on fitness and population dynamics. We studied populations of Daphnia dentifera to determine the amount of investment in sexual reproduction as well as the factors associated with variation in investment in sex. To do so, we tracked host density, infections by nine different parasites, and sexual reproduction in 15 lake populations of D. dentifera for 3 years. Sexual reproduction was seasonal, with male and ephippial female production beginning as early as late September and generally increasing through November. However, there was substantial variation in the prevalence of sexual individuals across populations, with some populations remaining entirely asexual throughout the study period and others shifting almost entirely to sexual females and males. We found strong relationships between density, prevalence of infection, parasite species richness, and sexual reproduction in these populations. However, strong collinearity between density, parasitism, and sexual reproduction means that further work will be required to disentangle the causal mechanisms underlying these relationships.     

Competitive exclusion and persistence in models of resource and sexual competition

 We study a combined mathematical model of resource and sexual competition. The population dynamics in this model is analyzed through a coupled system of reaction-diffusion equations. It is shown that strong sexual competition and low birth rate lead to competitive exclusion of the biological species. If sexual competition is weak, then the persistence of the species is possible, depending on the initial density functions and the growth rates of the species. When sexual competition affects both species, persistence and competitive exclusion results are also obtained in terms of the ecological data in the model. Received 1 November 1995; received in revised form 13 January 1996     

Loss and gain of sexual reproduction in the same stick insect

The outcome of competition between different reproductive strategies within a single species can be used to infer selective advantage of the winning strategy. Where multiple populations have independently lost or gained sexual reproduction it is possible to investigate whether the advantage is contingent on local conditions. In the New Zealand stick insect Clitarchus hookeri, three populations are distinguished by recent change in reproductive strategy and we determine their likely origins. One parthenogenetic population has established in the United Kingdom and we provide evidence that sexual reproduction has been lost in this population. We identify the sexual population from which the parthenogenetic population was derived, but show that the UK females have a post‐mating barrier to fertilisation. We also demonstrate that two sexual populations have recently arisen in New Zealand within the natural range of the mtDNA lineage that otherwise characterizes parthenogenesis in this species. We infer independent origins of males at these two locations using microsatellite genotypes. In one population, a mixture of local and nonlocal alleles suggested males were the result of invasion. Males in another population were most probably the result of loss of an X chromosome that produced a male phenotype in situ. Two successful switches in reproductive strategy suggest local competitive advantage for outcrossing over parthenogenetic reproduction. Clitarchus hookeri provides remarkable evidence of repeated and rapid changes in reproductive strategy, with competitive outcomes dependent on local conditions.     

Life-cycle switching and coexistence of species with no niche differentiation

The increasing evidence of coexistence of cryptic species with no recognized niche differentiation has called attention to mechanisms reducing competition that are not based on niche-differentiation. Only sex-based mechanisms have been shown to create the negative feedback needed for stable coexistence of competitors with completely overlapping niches. Here we show that density-dependent sexual and diapause investment can mediate coexistence of facultative sexual species having identical niches. We modelled the dynamics of two competing cyclical parthenogens with species-specific density-dependent sexual and diapause investment and either equal or different competitive abilities. We show that investment in sexual reproduction creates an opportunity for other species to invade and become established. This may happen even if the invading species is an inferior competitor. Our results suggests a previously unnoticed mechanism for species coexistence and can be extended to other facultative sexual species and species investing in diapause where similar density-dependent life-history switches could act to promote coexistence.     

长江中下游湖泊两种混生苦草属植物生活史特征与共存分布格局

 在对长江中下游流域湖南、湖北、江西和安徽4省25个湖泊苦草属(Vallisneria)植物种群进行广泛的取样调查、鉴定和查明种间共存格局的基 础上,结合同园种植实验,对该属两个混生近缘种刺苦草(V. spinulosa)和苦草(V. natans)有性和无性生活史特征进行了定量测定和比较研究 ,探讨了种间生活史差异对种间共存格局的影响。结果表明：1)刺苦草是长江中下游湖泊的优势物种,苦草为常见种,而密刺苦草(V. denseserrulata)仅有很少分布;2)苦草和刺苦草常混生于这些湖泊中,形成共存分布格局：刺苦草和苦草种间呈明显的的带状相间分布格局, 或苦草只零星分布于刺苦草群落中;3)刺苦草和苦草有性和无性生活史特征显著不同：刺苦草为多年生,主要以无性繁殖为主,只有有限的有 性繁殖投入;相反,苦草在调查的地区为一年生,以有性繁殖为主,只进行微弱的克隆生长,且不能产生克隆繁殖器官(冬芽)。刺苦草和苦草 在有性和无性繁殖生活史对策上的权衡,导致种间资源利用和竞争能力的分异而使这两个近缘种得以共存。     

Experimental manipulation of plant density and its effect on pollination and reproduction of two confamilial montane herbs

The density of a plant population is expected to influence reproductive success through changes in the quantity and quality of pollination service, or because both density and reproduction respond to quality of the local environment. We reported previously that seed set in sparse natural populations of Delphinium nuttallianum and Aconitum columbianum was lower than in nearby dense populations, whereas quantity of pollination service was equivalent. To explore the hypotheses that environmental quality or pollination quality are lower in sparse natural populations, leading to lower seed set, we manipulated density using arrays of potted plants. In three replicate experiments with D. nuttallianum, pollinator visitation rate and seed set were indistinguishable in sparse and dense arrays, consistent with the interpretation that environmental quality contributed to the earlier result in natural populations of this species. In three replicates with A. columbianum, visitation rate tended to increase with density, and seed set increased significantly, in contrast to our earlier result. One element of pollination quality, the degree of within-plant selfing, did not vary between sparse and dense arrays. These results highlight the complexity of mechanisms by which population parameters may influence plant reproductive success, and the temporal variation that characterizes pollination service.     

Temporal differentiation and spatial coexistence of sexual and facultative asexual lineages of an aphid species at mating sites

Cases of coexisting sexual and asexual relatives are puzzling, as evolutionary theory predicts that competition for the same ecological niches should lead to the exclusion of one or the other population. In the cyclically parthenogenetic aphid, Rhopalosiphum padi, sexual and facultative asexual lineages are admixed in space at the time of sexual reproduction. We investigated how the interaction of reproductive mode and environment can lead to temporal niche differentiation. We demonstrated theoretically that differential sensitivity of sexual and facultatively asexual aphids to an environmental parameter (mating host suitability) shapes the two strategies: whereas the sexual lineages switch earlier to the production of sexual forms, the facultative asexual lineages delay and spread out their investment in sexual reproduction. This predicted pattern of niche specialization is in agreement with the temporal structure revealed in natura by demographic and genetic data. We propose that partial loss of sex by one pool of aphids and subsequent reduction in gene flow between lineages may favour temporal specialization through disruptive selection.     

Daphnia females adjust sex allocation in response to current sex ratio and density

Cyclical parthenogenesis presents an interesting challenge for the study of sex allocation, as individuals’ allocation decisions involve both the choice between sexual and asexual reproduction, and the choice between sons and daughters. Male production is therefore expected to depend on ecological and evolutionary drivers of overall investment in sex, and those influencing male reproductive value during sexual periods. We manipulated experimental populations, and made repeated observations of natural populations over their growing season, to disentangle effects of population density and the timing of sex from effects of adult sex ratio on sex allocation in cyclically parthenogenetic Daphnia magna. Male production increased with population density, the major ecological driver of sexual reproduction; however, this response was dampened when the population sex ratio was more male‐biased. Thus, in line with sex ratio theory, we show that D. magna adjust offspring sex allocation in response to the current population sex ratio.     

Population size dependence, competitive coexistence and habitat destruction

1. Spatial dynamics can lead to coexistence of competing species even with strong asymmetric competition under the assumption that the inferior competitor is a better colonizer given equal rates of extinction. Patterns of habitat fragmentation may alter competitive coexistence under this assumption.
2. Numerical models were developed to test for the previously ignored effect of population size on competitive exclusion and on extinction rates for coexistence of competing species. These models neglect spatial arrangement.
3. Cellular automata were developed to test the effect of population size on competitive coexistence of two species, given that the inferior competitor is a better colonizer. The cellular automata in the present study were stochastic in that they were based upon colonization and extinction probabilities rather than deterministic rules.
4. The effect of population size on competitive exclusion at the local scale was found to have little consequence for the coexistence of competitors at the metapopulation (or landscape) scale. In contrast, population size effects on extinction at the local scale led to much reduced landscape scale coexistence compared to simulations not including localized population size effects on extinction, especially in the cellular automata models. Spatially explicit dynamics of the cellular automata vs. deterministic rates of the numerical model resulted in decreased survival of both species. One important finding is that superior competitors that are widespread can become extinct before less common inferior competitors because of limited colonization.
5. These results suggest that population size–extinction relationships may play a large role in competitive coexistence. These results and differences are used in a model structure to help reconcile previous spatially explicit studies which provided apparently different results concerning coexistence of competing species.     

Experimental evolution reveals differences between phenotypic and evolutionary responses to population density

Group living can select for increased immunity, given the heightened risk of parasite transmission. Yet, it also may select for increased male reproductive investment, given the elevated risk of female multiple mating. Trade‐offs between immunity and reproduction are well documented. Phenotypically, population density mediates both reproductive investment and immune function in the Indian meal moth, Plodia interpunctella. However, the evolutionary response of populations to these traits is unknown. We created two replicated populations of P. interpunctella, reared and mated for 14 generations under high or low population densities. These population densities cause plastic responses in immunity and reproduction: at higher numbers, both sexes invest more in one index of immunity [phenoloxidase (PO) activity] and males invest more in sperm. Interestingly, our data revealed divergence in PO and reproduction in a different direction to previously reported phenotypic responses. Males evolving at low population densities transferred more sperm, and both males and females displayed higher PO than individuals at high population densities. These positively correlated responses to selection suggest no apparent evolutionary trade‐off between immunity and reproduction. We speculate that the reduced PO activity and sperm investment when evolving under high population density may be due to the reduced population fitness predicted under increased sexual conflict and/or to trade‐offs between pre‐ and post‐copulatory traits.     

Yoyo-bang: a risk-aversion investment strategy by a perennial insect society

In 1978, Oster and Wilson proposed a bang-bang investment strategy for social insects in which colony size at maturity amplifies colony reproduction. In this paper, the investment strategies of the monogyne form of the fire ant, Solenopsis invicta, were compared to the predictions of the bang-bang model. Demographic census data, collected on fire ant mounds excavated every month during the years 1985 and 1988, revealed that colony reproduction was independent of colony size (~50,000 to ~250,000 workers). Why were mature S. invicta colonies up to five times larger than they needed to be to reproduce an annual batch of sexual offspring? To address this question, Oster and Wilson's bang-bang model was modified to a "yoyo-bang" investment strategy for perennial societies. In the yoyo-bang model, excess workers are a disposable reserve - a buffer - that can oscillate up or down depending on resource availability without adversely affecting annual reproductive cycles. The yoyo-bang model links colony size, colony survival and lifetime reproductive fitness.     

Sex and space destabilize intransitive competition within and between species

Organisms ranging from bacteria and corals to plants and vertebrates can form intransitive competitive networks, in which coexistence can be maintained because no one species or genotype is superior to all others. However, in the simplest case with three competing types, the long-term outcome may not be so clear if two of the three represent the ends of a continuous heritable trait distribution within one species, as has been recently demonstrated empirically in a short-term experiment with plants. Using simulation models of this scenario, results with asexual reproduction confirm previous studies which showed that local interactions promote coexistence. However, with sexual reproduction, genetic variance is reduced because selection fluctuates between favouring the two extremes during population cycles, while sex continually produces intermediates. Sex thus slows the response to selection when it is the strongest and therefore slows the recovery from extreme abundances, creating larger abundance fluctuations. Local interactions do not stabilize dynamics with sex because the resultant spatial patches of one species are genetically heterogeneous, such that particular phenotypes do not benefit from spatial refuges. In sharp contrast to previous models suggesting that sex or local interactions stabilize population dynamics, here sex and local interactions destabilize dynamics and increase extinction risk.     

Interspecific interactions change the outcome of sexual conflict over prehatching parental investment in the burying beetle Nicrophorus vespilloides

Sexual conflict arises when the optimal reproductive strategy differs for males and females. It is associated with every reproductive stage, yet few studies have considered how the outcome may be changed by interactions with other species. Here, we show that phoretic mites Poecilochirus carabi change the outcome of sexual conflict over the supply of prehatching parental investment in the burying beetle Nicrophorus vespilloides. Burying beetles require a small dead vertebrate for reproduction, which they prepare by shaving it, rolling up the flesh, and burying it. When pairs were given a medium‐sized mouse to prepare (13–16 g), mites changed how the costs of reproduction were divided between the sexes, with males then sustaining greater costs than females. We found no equivalent difference when pairs prepared larger or smaller carcasses. Thus, our experiment shows that the outcome of sexual conflict over prehatching parental investment is changed by interactions with other species during reproduction.     

Variability of patch type preferences in relation to resource availability and breeding success in a bird

This paper investigates how variability in partial foraging preferences for patch types can be used as a behavioral indicator of the energetic value of that patch type, and of overall food availability in the territory. The species studied was the lesser spotted woodpecker (Dendrocopos minor) and the patch types it uses are four groups of tree species (oak Quercus robur, birch Betula pendula, B. pubescens, alder Alnus glutinosa, and lime Tilia cordata), in which it feeds upon wood-living insect larvae. We partition the variation in foraging preferences into three scales. Firstly, within territories, the foraging preference for a tree species group was positively related to the prey density in that species group. That is, the preferences measure the patch types' energetic profitabilities. This result should be general in cases like the present, where the costs of using different alternatives do not differ substantially. It may therefore be the preferred behavioral indicator in determining the relative benefits associated with different alternatives. Secondly, between the seven years of study, much of the variation in tree species group preferences was attributable to measured fluctuations in the density of one important prey species (Argyresthia goedarthella, Argyresthidae, Lepidoptera), which occurred in some years on birch, in others on alder, and in one year was virtually absent. Thus, in concordance with the previous result, the values of these tree species groups fluctuated between years according to prey density. Thirdly, between territories, we found that the preference for one tree species, lime, was higher in areas where it was more abundant. We attribute this to the fact that the density (per patch) of at least one important prey species (Stenostola dubia, Cerambycidae, Coleoptera) on lime increased with the abundance of its host tree species in the territory. That is, the overall food availability was higher in territories where lime was more common. Hence, the preference for lime estimates overall food availability. This conclusion is strengthened by two additional facts: the preference for lime correlates positively (1) with the average giving-up density of food, which has previously been shown to estimate overall food availability in the territories, and (2) with reproductive success, at least during the early stages of reproduction.     

A comparison of native and invasive populations of three clonal plant species in Germany and New Zealand

Aim Our aim was to test for changes in growth patterns of three clonally growing plant species (Achillea millefolium, Hieracium pilosella and Hypericum perforatum) between native and invaded regions. We addressed the hypotheses that with differing important life‐history traits, invasive populations perform better than native populations, and that this expected better performance is linked to weakened trade‐offs between individual growth and sexual and clonal reproduction. Location Germany and New Zealand. Methods We conducted field surveys for the three above‐mentioned species in both native German and invasive New Zealand populations, and collected data at both population and individual levels. Results At the population level, the proportion of flowering plants, population size and population density were all higher in invasive populations. Similarly, at the individual level, the number of stolons per plant, stolon–biomass ratio and population crowdedness (local plant density in a specified area around a target plant) were significantly higher in New Zealand. Plant height did not differ between countries, and plant biomass was lower in New Zealand than in Germany for Achillea millefolium and Hypericum perforatum. These two species showed significant trade‐offs between individual growth and sexual and clonal reproduction. Achillea millefolium exhibited a weakened trade‐off in its invaded range, where the same proportion of flowering plants was sustained at much higher levels of population crowdedness than in its native range. Main conclusions The apparent invasion success of the three study species is generally due to better overall performance in their respective invaded ranges. In respect of both Achillea millefolium and Hypericum perforatum, this is driven primarily by increased vegetative reproduction. In contrast, Hieracium pilosella seems to benefit more from increased sexual reproduction in its invaded range. Shifts in trade‐offs as a general trend seem to be of minor importance.     

Sexual reproduction and population dynamics: the role of polygyny and demographic sex differences.

Most models of population dynamics do not take sexual reproduction into account (i.e., they do not consider the role of males). However, assumptions behind this practice--that no demographic sex differences exist and males are always abundant enough to fertilize all the females--are usually not justified in natural populations. On the contrary, demographic sex differences are common, especially in polygynous species. Previous models that consider sexual reproduction report a stabilizing effect through mixing of different genotypes, thus suggesting a decrease in the propensity for complex of dynamics in sexually reproducing populations. Here we show that considering the direct role of males in reproduction and density dependence leads to the conclusion that a two-sex model is not necessarily more stable compared with the corresponding one-sex model. Although solutions exist where sexual reproduction has a stabilizing effect even when no genotypic variability is included (primarily when associated with monogamy), factors like polygyny, sex differences in survival or density dependence, and possible alterations of the primary sex ratio (the Trivers-Willard mechanism), may enlarge the parametric region of complex dynamics. Sexual reproduction therefore does not necessarily increase the stability of population dynamics and can have destabilizing effects, at least in species with complicated mating systems and sexual dimorphism.