Sexual conflict and ecology: Species composition and male density interact to reduce male mating harassment and increase female survival

Sexual conflict is a pervasive evolutionary force that can reduce female fitness. Experimental evolution studies in the laboratory might overestimate the importance of sexual conflict because the ecological conditions in such settings typically include only a single species. Here, we experimentally manipulated conspecific male density (high or low) and species composition (sympatric or allopatric) to investigate how ecological conditions affect female survival in a sexually dimorphic insect, the banded demoiselle (Calopteryx splendens). Female survival was strongly influenced by an interaction between male density and species composition. Specifically, at low conspecific male density, female survival increased in the presence of heterospecific males (C. virgo). Behavioral mating experiments showed that interspecific interference competition reduced conspecific male mating success with large females. These findings suggest that reproductive interference competition between con‐ and heterospecific males might indirectly facilitate female survival by reducing mating harassment from conspecific males. Hence, interspecific competitors can show contrasting effects on the two sexes thereby influencing sexual conflict dynamics. Our results call for incorporation of more ecological realism in sexual conflict research, particularly how local community context and reproductive interference competition between heterospecific males can affect female fitness.     

Eavesdropping of an African ground squirrel on the heterospecific alarm calls of a noisy ground-nesting bird

Animals gather information about their environment from a variety of sources to enable adaptive decision-making behaviour. Eavesdropping on heterospecific alarm calls enhances predator avoidance, reduces time spent vigilant and allows for more time on daily activities such as foraging. If the information is relevant and reliable, individuals that respond to heterospecific signals may benefit from a wider range of information at a low marginal cost. The Cape ground squirrel (Xerus inauris) and crowned lapwing (Vanellus chilensis) are ground-dwelling species that are taxonomically distant but share similar predators, habitat and anti-predatory behaviours. We used playback experiments of the alarm calls produced by conspecifics and lapwings to investigate the vigilance responses of adult female Cape ground squirrels. Squirrels responded with greater vigilance to both squirrel and lapwing alarm calls, and no changes of vigilance levels were observed in response to a control sound. However, contrary to our predictions, changes in vigilance and time to relax did not differ between conspecific versus heterospecific playbacks. The results from our study suggest that squirrels perceive lapwing alarm calls as relevant and reliable information and that responding to it could increase their survival.     

Sexual differentiation and seasonal variation in response to conspecific and heterospecific acoustic signals

Interspecific territoriality is frequently reported between closely related species; however, few studies have demonstrated interspecific territoriality between distantly related species living in sympatry. We conducted playback experiments to investigate territorial behaviour in male and female White‐bellied Wrens (Uropsila leucogastra) in response to simulated conspecific and heterospecific intruders during the breeding and non‐breeding seasons. We explored whether heterospecific songs of the Happy Wren (Pheugopedius felix), a distantly related species and ecological competitor, elicited antagonistic responses from focal White‐bellied Wrens, and whether such responses differed between the sexes. We also examined whether male and female responses to conspecific and heterospecific rivals varied with season. We found that male White‐bellied Wrens always responded to conspecific song, and responded significantly more to heterospecific song compared to a control stimulus (Tropical Parula, Setophaga pitiayumi). In contrast, although female White‐bellied Wrens responded strongly to conspecific song, their response to heterospecific song did not differ significantly from the control stimulus. The proportion of males that responded to heterospecific songs and the proportion of females that responded to conspecific songs varied seasonally, showing significantly lower responses during the breeding season. The intense responses of male White‐bellied Wrens to playback of heterospecific songs suggest that they recognise ecological competitors based on their vocal signals. Furthermore, the decrease in agonistic interactions during the breeding season is in line with the hypothesis that aggressive behaviour may be detrimental to reproductive and parental activity, and the hypothesis that heterospecific animals pose less of a threat during the breeding season.     

Nitrogen fixation and nitrogen limitation of primary production along a natural marsh chronosequence

We experimentally tested the conditions where heterospecific attraction is more likely to occur. The heterospecific attraction hypothesis predicts that colonizing or migrant individuals use the presence of resident species as a cue for profitable breeding sites. In other words, increasing resident densities will result in increased migrant densities until the costs of interspecific competition override the benefits of heterospecific attraction. The experiment consisted of a reference and a manipulation year. In the reference year, resident titmice were permitted to breed at intermediate densities whilst in the manipulation year, resident densities were manipulated in nine study plots. Three treatments were performed as low, intermediate and high resident densities and migrant density responses were measured in both years. Relative between-year migrant and resident densities were analyzed by regression analysis. Migrant foliage gleaning guild densities responded linearly and positively, as did densities of habitat generalists, in particular Chaffinch ( Fringilla coelebs),. The ground-foraging guild did not show a response. This study provides support for predictions of the heterospecific attraction hypothesis and suggests that information on habitat quality with reference to both food availability and safe breeding sites are important in using heterospecifics as cues. Based on Chaffinch response data, artificially increased resident densities were not high enough for competitive effects between residents and migrants to decrease heterospecific attraction. It seems unlikely that in northern environments natural resident densities will reach high levels where competitive effects would occur, therefore heterospecific attraction will always be beneficial. This study again shows the importance of heterospecific attraction in migrant habitat selection and as a process promoting species diversity in northern breeding bird assemblages.     

Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification.

Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect-microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.     

PHYTOPHAGOUS INSECT–MICROBE MUTUALISMS AND ADAPTIVE EVOLUTIONARY DIVERSIFICATION

Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect–microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.     

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.     

Mycorrhizal feedback is not associated with the outcome of competition in old‐field perennial plants

The symbiosis between plants and arbuscular mycorrhizal (AM) fungi is hypothesized to be an important contributor to plant–soil feedbacks, which can influence the outcome of inter‐specific competition. Mycorrhizal feedbacks can be conspecific, which affects individuals of the same species, or heterospecific, which affects individuals of a different species. When heterospecific feedbacks are more positive than conspecific feedbacks, heterospecific individuals are expected to outcompete conspecific individuals. To test this hypothesis, we quantified conspecific mycorrhizal feedback for Plantago lanceolata as a focal species, and heterospecific mycorrhizal feedbacks for 21 competitor old‐field species using mycorrhizae cultured with P. lanceolata. We quantified inter‐specific competition against the focal species by growing the 21 old‐field species with and without P. lanceolata in the presence of mycorrhizae cultured with P. lanceolata. Heterospecific and conspecific feedbacks were both positive, and average heterospecific feedbacks exceeded conspecific feedback by 75%. Competition suppressed P. lanceolata biomass by 14% and average competitor biomass was reduced by 44% in the presence of P. lanceolata, and these effects varied with competitor species identity. Contrary to predictions, the magnitude of heterospecific feedbacks did not predict the ability of competitor species to either suppress or resist suppression by P. lanceolata. Instead, the outcome of competition was significantly and positively correlated with intrinsic growth rate, measured as biomass of competitor species five weeks after germination in non‐inoculated conditions. Our findings suggest that species experiencing more positive mycorrhizal feedbacks than a competitor do not necessarily have a competitive advantage. Mycorrhizal mediated soil feedbacks may be less important than intrinsic differences in growth rate in determining competitive outcomes.     

Quantifying the Adaptive Cycle

The adaptive cycle was proposed as a conceptual model to portray patterns of change in complex systems. Despite the model having potential for elucidating change across systems, it has been used mainly as a metaphor, describing system dynamics qualitatively. We use a quantitative approach for testing premises (reorganisation, conservatism, adaptation) in the adaptive cycle, using Baltic Sea phytoplankton communities as an example of such complex system dynamics. Phytoplankton organizes in recurring spring and summer blooms, a well-established paradigm in planktology and succession theory, with characteristic temporal trajectories during blooms that may be consistent with adaptive cycle phases. We used long-term (1994–2011) data and multivariate analysis of community structure to assess key components of the adaptive cycle. Specifically, we tested predictions about: reorganisation: spring and summer blooms comprise distinct community states; conservatism: community trajectories during individual adaptive cycles are conservative; and adaptation: phytoplankton species during blooms change in the long term. All predictions were supported by our analyses. Results suggest that traditional ecological paradigms such as phytoplankton successional models have potential for moving the adaptive cycle from a metaphor to a framework that can improve our understanding how complex systems organize and reorganize following collapse. Quantifying reorganization, conservatism and adaptation provides opportunities to cope with the intricacies and uncertainties associated with fast ecological change, driven by shifting system controls. Ultimately, combining traditional ecological paradigms with heuristics of complex system dynamics using quantitative approaches may help refine ecological theory and improve our understanding of the resilience of ecosystems.     

Reproductive interference between animal species

Although sexual interactions between species (reproductive interference) have been reported from a wide range of animal taxa, their potential for determining species coexistence is often disregarded. Here, we review evidence from laboratory and field studies illustrating that heterospecific sexual interactions are frequently associated with fitness loss and can have severe ecological and evolutionary consequences. We define reproductive interference as any kind of interspecific interaction during the process of mate acquisition that adversely affects the fitness of at least one of the species involved and that is caused by incomplete species recognition. We distinguish seven types of reproductive interference: signal jamming, heterospecific rivalry, misdirected courtship, heterospecific mating attempts, erroneous female choice, heterospecific mating, and hybridization. We then discuss the sex-specific costs of these types and highlight two typical features of reproductive interference: density-dependence and asymmetry. Similar to competition, reproductive interference can lead to displacement of one species (sexual exclusion), spatial, temporal, or habitat segregation, changes in life history parameters, and reproductive character displacement. In many cases, patterns of coexistence might be shaped by reproductive interference rather than by resource competition, as the presence of a few heterospecifics might substantially decrease reproductive success. Therefore, interspecific sexual interactions should receive more attention in ecological research. Reproductive interference has mainly been discussed in the context of invasive species or hybrid zones, whereas its influence on naturally-occurring sympatric species pairs has rarely been addressed. To improve our knowledge of the ecological significance of reproductive interference, findings from laboratory experiments should be validated in the field. Future studies should also focus on ecological mechanisms, such as temporal spatial, or habitat partitioning, that might enable sexually interacting species to coexist. Reproductive interference also has implications for the management of endangered species, which can be threatened by sexual interactions with invasive or common species. Studies of reproductive interference might even provide new insights for biological pest control.     

Breaking down the Species Boundaries: Selective Pressures behind Interspecific Communication in Vertebrates

Studying heterospecific communication provides an opportunity to examine the dynamics of cross‐species social behaviour. It allows us to ask questions about the extent to which the transfer of information is adaptive or accidental and provides an empirically tractable context for manipulating relationships. To date, most studies of heterospecific communication have focussed on receivers. However, the selective pressures on signallers can be as important in determining the dynamics of interspecific communication. Here, we propose a simple framework for thinking about cross‐species information transfer, which (i) considers whether information exchange is either accidental or adaptive and (ii) whether it is unidirectional or bidirectional. To clearly classify interactions, it is necessary to quantify all of the payoffs of interspecific communication to both signallers and receivers. This requires accurate characterisation of the currency influenced by cross‐species communication (e.g. weight gain, foraging success, survival). However, quantifying the payoffs may be difficult, because each side may be benefiting via different currencies. To date, studies on heterospecific communication have focussed on only one dimension of a niche (usually antipredator or foraging signals). However, because niches are multidimensional, investigations should incorporate multiple aspects of a species’ niche, to get a better perspective on why we see certain patterns of information use between species.     

How ecology shapes caste evolution: linking resource use,morphology, performance and fitness in a superorganism

Caste evolution is a central process in the adaptive diversification of insect superorganisms. Nevertheless, how ecology shapes adaptive caste evolution remains poorly understood. Recent work with the ant genus Cephalotes has provided new comparative evidence that ecological specialization may drive adaptive caste specialization. Here, three key predictions of this adaptive hypothesis are supported, using a representative of the highest level of ecological specialization and the most specialized soldier phenotype. First, soldier defensive performance was maximal for the specific nesting resource used most often in nature. Second, colonies only used a specialized subset of available nesting resources and preferred the specific resource that maximizes soldier performance. Third, soldier performance and its limitations on resource use were found to have both direct and indirect consequences for colony reproduction. These findings suggest that the most specialized soldier phenotype in Cephalotes is indeed an adaptation to ecological specialization on a narrowly defined subset of available nesting resources.     

Species importance in a heterospecific foraging association network

There is a growing recognition of the need to integrate non‐trophic interactions into ecological networks for a better understanding of whole‐community organization. To achieve this, the first step is to build networks of individual non‐trophic interactions. In this study, we analyzed a network of interdependencies among bird species that participated in heterospecific foraging associations (flocks) in an evergreen forest site in the Western Ghats, India. We found the flock network to contain a small core of highly important species that other species are strongly dependent on, a pattern seen in many other biological networks. Further, we found that structural importance of species in the network was strongly correlated to functional importance of species at the individual flock level. Finally, comparisons with flock networks from other Asian forests showed that the same taxonomic groups were important in general, suggesting that species importance was an intrinsic trait and not dependent on local ecological conditions. Hence, given a list of species in an area, it may be possible to predict which ones are likely to be important. Our study provides a framework for the investigation of other heterospecific foraging associations and associations among species in other non‐trophic contexts.     

Heterospecific aggression and adaptive divergence in brook stickleback (Culaea inconstans)

Agonistic behavior between heterospecifics, in which individuals of one species attack another, may cause a subordinate species to shift resource or habitat use. Subsequent evolutionary responses to selection may mimic shifts expected under ecological character displacement, but with no role played by exploitative competition. Alternatively, aggressive behavior can evolve when fitness is improved by excluding members of a coexisting species from a defendable resource through interference. We tested whether heterospecific agonistic behavior has evolved in brook stickleback (Culaea inconstans) by comparing replicate allopatric populations to those sympatric with ninespine stickleback (Pungitius pungitius). We also tested for heritable variation in heterospecific aggressive behavior by rearing family groups in a common environment. Allopatric populations of brook stickleback were more aggressive than ninespine stickleback, suggesting that pre-existing aggression in brook stickleback contributed to niche shifts by ninespine stickleback. In addition, sympatric adult brook stickleback were more aggressive toward ninespine stickleback than brook stickleback from allopatric populations. Overt heterospecific aggressive behaviors were heritable, and aggression in juvenile brook stickleback increased with age in sympatric but not in allopatric populations reared in a common environment. Brook stickleback have evolved increased aggression when they coexist with ninespine stickleback. These stickleback communities have been structured by both evolved and pre-existing variation in heterospecific aggressive behavior in brook stickleback.     

Learning decreases heterospecific courtship and mating in fruit flies

Recent theory and data suggest that adaptive use of learning in the context of sexual behaviour could contribute to assortative mating. Experiments examining this issue indicated that male Drosophila persimilis that experienced courtship and rejection by heterospecific females exhibited significantly lower levels of heterospecific courtship and mating compared with those of inexperienced males. These results indicate that experience in the context of sexual behaviour in fruit flies could reduce gene flow between diverging populations, which may contribute to incipient speciation.     

A biogeographic genetic approach for testing the role of reinforcement: the case of Drosophila pseudoobscura and D. persimilis

Abstract.— The role of reinforcement in speciation can be explained by two distinct models. In model I, two diverged populations hybridize and produce fertile hybrids that successfully backcross (hybridization with gene flow). In model II, two populations hybridize but succeeding backcrosses are unproductive (hybridization without gene flow). Using Drosophila persimilis and D. pseudoobscura , we have tested model I by comparing the extent of heterospecific introgression in sympatric versus allopatric populations. We show that certain expectations of this particular model of reinforcement, which is based on hybridization and gene flow between divergent populations after secondary contact, are not realized in these two species. The evidence consists of the similarity of genetic distances as well as proportions of unique/rare alleles between sympatric and allopatric heterospecific populations and a negative correlation between genetic distance and geographical distance between heterospecific populations, which suggests ecological differentiation. This approach in quantifying differential gene flow has important consequences to studies that compare sympatric and allopatric isolation using genetic distance. Following model I, one would expect a pattern of higher prezygotic isolation in sympatric species compared to allopatric species of the same genetic distance simply as a result of an underestimation of genetic distance due to introgression between sympatric populations. We suggest more parsimonious explanations such as reinforcement without genetic exchange (model II) and ecological differentiation, which require high levels of preexisting reproductive isolation between populations.     

Ecological character displacement caused by reproductive interference

We carried out a theoretical investigation of whether ecological character displacement can be caused by reproductive interference. Our model assumes that a quantitative character is associated with both resource use and species recognition, and that heterospecific mating incurs costs. The model shows that ecological character displacement can occur as a consequence of evolution of premating isolation; this conclusion is based on the premise that resource competition is less intense between species than within species and that the ecological character also contributes to premating isolation. When resource competition between species is intense, extinction of either species may occur by competitive exclusion before ecological character divergence. Some observational studies have shown that character displacement in body size is associated with not only resources use but also species recognition. We propose that body size displacement can occur as a consequence of evolution of premating isolation. Our results suggest that ecological character displacement results from reproductive character displacement.     

Eco-evolutionary feedbacks,adaptive dynamics and evolutionary rescue theory

Adaptive dynamics theory has been devised to account for feedbacks between ecological and evolutionary processes. Doing so opens new dimensions to and raises new challenges about evolutionary rescue. Adaptive dynamics theory predicts that successive trait substitutions driven by eco-evolutionary feedbacks can gradually erode population size or growth rate, thus potentially raising the extinction risk. Even a single trait substitution can suffice to degrade population viability drastically at once and cause ‘evolutionary suicide’. In a changing environment, a population may track a viable evolutionary attractor that leads to evolutionary suicide, a phenomenon called ‘evolutionary trapping’. Evolutionary trapping and suicide are commonly observed in adaptive dynamics models in which the smooth variation of traits causes catastrophic changes in ecological state. In the face of trapping and suicide, evolutionary rescue requires that the population overcome evolutionary threats generated by the adaptive process itself. Evolutionary repellors play an important role in determining how variation in environmental conditions correlates with the occurrence of evolutionary trapping and suicide, and what evolutionary pathways rescue may follow. In contrast with standard predictions of evolutionary rescue theory, low genetic variation may attenuate the threat of evolutionary suicide and small population sizes may facilitate escape from evolutionary traps.     

Interspecific Pollen Transfer: Magnitude,Prevalence and Consequences for Plant Fitness

Interspecific pollen transfer (IPT) is one of the mechanisms underlying potential competition among plants for pollinators, and it refers to movement of pollen between different plant species by pollinators that visit their flowers simultaneously. Two components of IPT, related to each other, are distinguished: (a) heterospecific pollen deposition (HPD) on conspecific stigmas, which may interfere with fertilization by conspecific pollen; and (b) conspecific pollen loss (CPL) on heterospecific flowers, which may reduce the amount of pollen transferred between conspecific flowers. Thus, IPT may lead to reciprocal losses for male and female functions of the plant, with potentially important ecological and evolutionary consequences. In this review, we explore the magnitude and prevalence of IPT, examining documented mechanisms and evaluating such potential ecological and evolutionary consequences. We compiled existing evidence of interspecific pollinator sharing and interspecific pollinator switching between flowers of different species in natural communities. We evaluated the relative importance of both HPD and CPL from studies comparing these variables in pure vs. mixed floral neighborhoods, analyzing evidence for the claim that IPT is an evolutionary force promoting character displacement in habitat affinity, flowering times, and floral morphology. We also examined the findings of hand-pollination experiments carried out to reveal different mechanisms by which heterospecific pollen can affect performance of native pollen. Finally, we review evidence for impacts of alien plant species on native species' reproduction, and briefly comment on risks of crop-to-wild gene flow imposed by the release of genetically modified (transgenic) crops through IPT.     

Common-garden studies on adaptive radiation of photosynthetic physiology among Hawaiian lobeliads

Species in an adaptive radiation often occupy different habitats so that individuals of each species develop under different conditions. Showing that a radiation is adaptive thus requires evidence that taxa have diverged genetically and that each has an ecological advantage in using particular habitats or resources, taking into account both phenotypic plasticity and phylogenetic relationships among species. Here, we use a common-garden experiment to show that representative species of Hawaiian lobeliads have diverged adaptively in their leaf-level photosynthetic light responses. Across species, plants genetically shifted their photosynthetic physiology with native light regime in accord with theoretical predictions and exhibited adaptive crossover in net carbon gain—that is, species native to a given light regime outperformed others only under conditions similar to those they occupy in the field, with the rank order of species based on photosynthesis per unit leaf mass changing with light level. These findings make a powerful case for adaptation of photosynthetic light responses to native light regimes and, combined with our earlier field studies, provide the strongest demonstration to date for the evolution of divergent adaptations for energy capture in any group of closely related plants.