Kenichi W. Okamoto

The role of interspecific interference competition in character displacement and the evolution of competitor recognition.

The extent to which interspecific interference competition has contributed to character evolution is one of the most neglected problems in evolutionary biology. When formerly allopatric species come into secondary contact, aggressive interactions between the species can cause selection on traits that affect interspecific encounter rates (e.g. habitat preferences, activity schedules), competitor recognition (e.g. colouration, song), and fighting ability (e.g. weaponry, body size). We define agonistic character displacement (ACD) as the process of phenotypic evolution in a population caused by interference competition with one or more sympatric species and which results in shifts in traits that affect the rate, intensity or outcome of interspecific aggression. After clarifying the relationships between ACD and other evolutionary processes that may occur when species come into secondary contact, we develop an individual‐based, quantitative genetic model to examine how traits involved in competitor recognition would be expected to evolve under different secondary contact scenarios. Our simulation results show that both divergence and convergence are possible outcomes, depending on the intensity of interspecific exploitative competition, the costs associated with mutual versus unilateral recognition, and the extent of phenotypic differences prior to secondary contact. We then devise a set of eight criteria for evaluating putative examples of ACD and review the empirical literature to assess the strength of existing evidence and to identify promising avenues for future research. Our literature search revealed 33 putative examples of ACD across insects, fishes, bats, birds, lizards, and amphibians (15 divergence examples; 18 convergence examples). Only one example satisfies all eight criteria for demonstrating ACD, but most case studies satisfy four or more criteria. The current state of the evidence for ACD is similar to the state of the evidence for ecological character displacement just 10 years ago. We conclude by offering suggestions for further theoretical and empirical research on ACD.

The evolutionary consequences of interspecific aggression

Competition has always been a cornerstone of evolutionary biology, and aggression is the predominant form of direct competition in animals, but the evolutionary effects of aggression between species are curiously understudied. Only in the past few years, existing theoretical frameworks have been extended to include interspecific aggression, and significant empirical advances have been made. After arguing that agonistic character displacement (ACD) theory provides the most suitable theoretical framework, we review new empirical evidence for ACD and the results of mathematical models of the process. We consider how ACD can be distinguished empirically from ecological and reproductive character displacement and the additional challenges posed by developmental plasticity. We also provide the first taxonomically broad review of theoretical and empirical work on the effects of interspecific aggression on species coexistence and range limits. We conclude by highlighting promising directions for future research on the evolutionary effects of interspecific aggression.

Mitigating fisheries-induced evolution in lacustrine brook charr (Salvelinus fontinalis) in southern Quebec, Canada.

Size‐selective mortality caused by fishing can impose strong selection on harvested fish populations, causing evolution in important life‐history traits. Understanding and predicting harvest‐induced evolutionary change can help maintain sustainable fisheries. We investigate the evolutionary sustainability of alternative management regimes for lacustrine brook charr (Salvelinus fontinalis) fisheries in southern Canada and aim to optimize these regimes with respect to the competing objectives of maximizing mean annual yield and minimizing evolutionary change in maturation schedules. Using a stochastic simulation model of brook charr populations consuming a dynamic resource, we investigate how harvesting affects brook charr maturation schedules. We show that when approximately 5% to 15% of the brook charr biomass is harvested, yields are high, and harvest‐induced evolutionary changes remain small. Intensive harvesting (at approximately >15% of brook charr biomass) results in high average yields and little evolutionary change only when harvesting is restricted to brook charr larger than the size at 50% maturation probability at the age of 2 years. Otherwise, intensive harvesting lowers average yield and causes evolutionary change in the maturation schedule of brook charr. Our results indicate that intermediate harvesting efforts offer an acceptable compromise between avoiding harvest‐induced evolutionary change and securing high average yields.

The evolution of species recognition in competitive and mating contexts: the relative efficacy of alternative mechanisms of character displacement.

Sympatric divergence in traits affecting species recognition can result from selection against cross-species mating (reproductive character displacement, RCD) or interspecific aggression (agonistic character displacement, ACD). When the same traits are used for species recognition in both contexts, empirically disentangling the relative contributions of RCD and ACD to observed character shifts may be impossible. Here, we develop a theoretical framework for partitioning the effects of these processes. We show that when both mate and competitor recognition depend on the same trait, RCD sets the pace of character shifts. Moreover, RCD can cause divergence in competitor recognition, but ACD cannot cause divergence in mate recognition. This asymmetry arises because males with divergent recognition traits may avoid needless interspecific conflicts, but suffer reduced attractiveness to conspecific females. Therefore, the key empirical issue is whether the same or different traits are used for mate recognition and competitor recognition.

Reproductive interference explains persistence of aggression between species

Interspecific territoriality occurs when individuals of different species fight over space, and may arise spontaneously when populations of closely related territorial species first come into contact. But defence of space is costly, and unless the benefits of excluding heterospecifics exceed the costs, natural selection should favour divergence in competitor recognition until the species no longer interact aggressively. Ordinarily males of different species do not compete for mates, but when males cannot distinguish females of sympatric species, females may effectively become a shared resource. We model how reproductive interference caused by undiscriminating males can prevent interspecific divergence, or even cause convergence, in traits used to recognize competitors. We then test the model in a genus of visually orienting insects and show that, as predicted by the model, differences between species pairs in the level of reproductive interference, which is causally related to species differences in female coloration, are strongly predictive of the current level of interspecific aggression. Interspecific reproductive interference is very common and we discuss how it may account for the persistence of interspecific aggression in many taxonomic groups.

A Reduce and Replace Strategy for Suppressing Vector-Borne Diseases: Insights from a Deterministic Model

Genetic approaches for controlling disease vectors have aimed either to reduce wild-type populations or to replace wild-type populations with insects that cannot transmit pathogens. Here, we propose a Reduce and Replace (R&R) strategy in which released insects have both female-killing and anti-pathogen genes. We develop a mathematical model to numerically explore release strategies involving an R&R strain of the dengue vector Aedes aegypti. We show that repeated R&R releases may lead to a temporary decrease in mosquito population density and, in the absence of fitness costs associated with the anti-pathogen gene, a long-term decrease in competent vector population density. We find that R&R releases more rapidly reduce the transient and long-term competent vector densities than female-killing releases alone. We show that releases including R&R females lead to greater reduction in competent vector density than male-only releases. The magnitude of reduction in total and competent vectors depends upon the release ratio, release duration, and whether females are included in releases. Even when the anti-pathogen allele has a fitness cost, R&R releases lead to greater reduction in competent vectors than female-killing releases during the release period; however, continued releases are needed to maintain low density of competent vectors long-term. We discuss the results of the model as motivation for more detailed studies of R&R strategies.

Assessing the Feasibility of Controlling Aedes aegypti with Transgenic Methods: A Model-Based Evaluation

Suppression of dengue and malaria through releases of genetically engineered mosquitoes might soon become feasible. Aedes aegypti mosquitoes carrying a conditionally lethal transgene have recently been used to suppress local vector populations in small-scale field releases. Prior to releases of transgenic insects on a wider scale, however, most regulatory authorities will require additional evidence that suppression will be effective in natural heterogeneous habitats. We use a spatially explicit stochastic model of an Ae. aegypti population in Iquitos, Peru, along with an uncertainty analysis of its predictions, to quantitatively assess the outcome of varied operational approaches for releases of transgenic strains with conditional death of females. We show that population elimination might be an unrealistic objective in heterogeneous populations. We demonstrate that substantial suppression can nonetheless be achieved if releases are deployed in a uniform spatial pattern using strains combining multiple lethal elements, illustrating the importance of detailed spatial models for guiding genetic mosquito control strategies.

A Reduce and Replace Strategy for Suppressing Vector-Borne Diseases: Insights from a Stochastic, Spatial Model

Two basic strategies have been proposed for using transgenic Aedes aegypti mosquitoes to decrease dengue virus transmission: population reduction and population replacement. Here we model releases of a strain of Ae. aegypti carrying both a gene causing conditional adult female mortality and a gene blocking virus transmission into a wild population to assess whether such releases could reduce the number of competent vectors. We find this “reduce and replace” strategy can decrease the frequency of competent vectors below 50% two years after releases end. Therefore, this combined approach appears preferable to releasing a strain carrying only a female-killing gene, which is likely to merely result in temporary population suppression. However, the fixation of anti-pathogen genes in the population is unlikely. Genetic drift at small population sizes and the spatially heterogeneous nature of the population recovery after releases end prevent complete replacement of the competent vector population. Furthermore, releasing more individuals can be counter-productive in the face of immigration by wild-type mosquitoes, as greater population reduction amplifies the impact wild-type migrants have on the long-term frequency of the anti-pathogen gene. We expect the results presented here to give pause to expectations for driving an anti-pathogen construct to fixation by relying on releasing individuals carrying this two-gene construct. Nevertheless, in some dengue-endemic environments, a spatially heterogeneous decrease in competent vectors may still facilitate decreasing disease incidence.

Feasible introgression of an anti-pathogen transgene into an urban mosquito population without using gene-drive.

Background Introgressing anti-pathogen constructs into wild vector populations could reduce disease transmission. It is generally assumed that such introgression would require linking an anti-pathogen gene with a selfish genetic element or similar technologies. Yet none of the proposed transgenic anti-pathogen gene-drive mechanisms are likely to be implemented as public health measures in the near future. Thus, much attention now focuses instead on transgenic strategies aimed at mosquito population suppression, an approach generally perceived to be practical. By contrast, aiming to replace vector competent mosquito populations with vector incompetent populations by releasing mosquitoes carrying a single anti-pathogen gene without a gene-drive mechanism is widely considered impractical. Methodology/Principal Findings Here we use Skeeter Buster, a previously published stochastic, spatially explicit model of Aedes aegypti to investigate whether a number of approaches for releasing mosquitoes with only an anti-pathogen construct would be efficient and effective in the tropical city of Iquitos, Peru. To assess the performance of such releases using realistic release numbers, we compare the transient and long-term effects of this strategy with two other genetic control strategies that have been developed in Ae. aegypti: release of a strain with female-specific lethality, and a strain with both female-specific lethality and an anti-pathogen gene. We find that releasing mosquitoes carrying only an anti-pathogen construct can substantially decrease vector competence of a natural population, even at release ratios well below that required for the two currently feasible alternatives that rely on population reduction. Finally, although current genetic control strategies based on population reduction are compromised by immigration of wild-type mosquitoes, releasing mosquitoes carrying only an anti-pathogen gene is considerably more robust to such immigration. Conclusions/Significance Contrary to the widely held view that transgenic control programs aimed at population replacement require linking an anti-pathogen gene to selfish genetic elements, we find releasing mosquitoes in numbers much smaller than those considered necessary for transgenic population reduction can result in comparatively rapid and robust population replacement. In light of this non-intuitive result, directing efforts to improve rearing capacity and logistical support for implementing releases, and reducing the fitness costs of existing recombinant technologies, may provide a viable, alternative route to introgressing anti-pathogen transgenes under field conditions.

The biological control of disease vectors.

Vector-borne diseases are common in nature and can have a large impact on humans, livestock and crops. Biological control of vectors using natural enemies or competitors can reduce vector density and hence disease transmission. However, the indirect interactions inherent in host-vector disease systems make it difficult to use traditional pest control theory to guide biological control of disease vectors. This necessitates a conceptual framework that explicitly considers a range of indirect interactions between the host-vector disease system and the vectors biological control agent. Here we conduct a comparative analysis of the efficacy of different types of biological control agents in controlling vector-borne diseases. We report three key findings. First, highly efficient predators and parasitoids of the vector prove to be effective biological control agents, but highly virulent pathogens of the vector also require a high transmission rate to be effective. Second, biocontrol agents can successfully reduce long-term host disease incidence even though they may fail to reduce long-term vector densities. Third, inundating a host-vector disease system with a natural enemy of the vector has little or no effect on reducing disease incidence, but inundating the system with a competitor of the vector has a large effect on reducing disease incidence. The comparative framework yields predictions that are useful in developing biological control strategies for vector-borne diseases. We discuss how these predictions can inform ongoing biological control efforts for host-vector disease systems.