Corlett W. Wood

Fitness consequences of social network position in a wild population of forked fungus beetles (Bolitotherus cornutus).

Social networks describe the pattern of intraspecific interactions within a population. An individual’s position in a social network often is expected to influence its fitness, but only a few studies have examined this relationship in natural populations. We investigated the fitness consequences of network position in a wild beetle population. Copulation success of male beetles positively covaried with strength (a measure of network centrality) and negatively covaried with clustering coefficient (CC) (a measure of cliquishness). Further analysis using mediation path models suggested that the activity level of individuals drove the relationships between strength and fitness almost entirely. In contrast, selection on CC was not explained by individual behaviours. Although our data suggest that social network position can experience strong sexual selection, it is also clear that the relationships between fitness and some network metrics merely reflect variation in individual‐level behaviours.

PHENOTYPIC ASSORTMENT MEDIATES THE EFFECT OF SOCIAL SELECTION IN A WILD BEETLE POPULATION

Social interactions often have major fitness consequences, but little is known about how specific interacting phenotypes affect the strength of natural selection. Social influences on the evolutionary process can be assessed using a multilevel selection approach that partitions the effects of social partner phenotypes on fitness (referred to as social or group selection) from those of the traits of a focal individual (nonsocial or individual selection). To quantify the contribution of social selection to total selection affecting a trait, the patterns of phenotypic association among interactants must also be considered. We estimated selection gradients on male body size in a wild population of forked fungus beetles (Bolitotherus cornutus). We detected positive nonsocial selection and negative social selection on body size operating through differences in copulation success, indicating that large males with small social partners had highest fitness. In addition, we found that, in low‐density demes, the phenotypes of focal individuals were negatively correlated with those of their social partners. This pattern reversed the negative effect of group selection on body size and led to stronger positive selection for body size. Our results demonstrate multilevel selection in nature and stress the importance of considering social selection whenever conspecific interactions occur nonrandomly.

Using home range estimates to construct social networks for species with indirect behavioral interactions

Social network analysis has become a vital tool for studying patterns of individual interactions that influence a variety of processes in behavior, ecology, and evolution. Taxa in which interactions are indirect or whose social behaviors are difficult to observe directly are being excluded from this rapidly expanding field. Here, we introduce a method that uses a probabilistic and spatially implicit technique for delineating social interactions. Kernel density estimators (KDE) are nonparametric techniques that are often used in home range analyses and allow researchers studying social networks to generate interaction matrices based on shared space use. We explored the use of KDE analysis and the effects of altering KDE input parameters on social network metrics using data from a natural population of the spatially persistent forked fungus beetle, Bolitotherus cornutus.

Consistency of animal social networks after disturbance

Social networks encompass both individual and group phenotypes that have been shown to covary with fitness in several species. In order for network characters to be evolutionarily important, they must reliably reflect properties of an individual or groups of individuals; however, it is unknown whether network traits are consistently expressed at either level. To determine if measurable components of individual social network position were repeatable and if the network structure as a whole was consistent in Bolitotherus cornutus (the forked fungus beetle), we constructed 8 experimental populations. Half of the populations were disturbed between 2 observation periods. Two individual network metrics (strength and betweenness) were significantly repeatable across time in all treatments; a third (clustering coefficient) was not. At the network level, all 3 metrics changed more in undisturbed than disturbed networks. These findings suggest that individual network position can be a consistent property of individuals that is resilient to disturbance and could experience selection in a predictable fashion. However, group network structure seems to change over time unless reset by disturbance.

Evolutionary response when selection and genetic variation covary across environments

Although models of evolution usually assume that the strength of selection on a trait and the expression of genetic variation in that trait are independent, whenever the same ecological factor impacts both parameters, a correlation between the two may arise that accelerates trait evolution in some environments and slows it in others. Here, we address the evolutionary consequences and ecological causes of a correlation between selection and expressed genetic variation. Using a simple analytical model, we show that the correlation has a modest effect on the mean evolutionary response and a large effect on its variance, increasing among-population or among-generation variation in the response when positive, and diminishing variation when negative. We performed a literature review to identify the ecological factors that influence selection and expressed genetic variation across traits. We found that some factors - temperature and competition - are unlikely to generate the correlation because they affected one parameter more than the other, and identified others - most notably, environmental novelty - that merit further investigation because little is known about their impact on one of the two parameters. We argue that the correlation between selection and genetic variation deserves attention alongside other factors that promote or constrain evolution in heterogeneous landscapes.

Nondestructive sampling of insect DNA from defensive secretion

Nondestructive techniques to obtain DNA from organisms can further genetic analyses such as estimating genetic diversity, dispersal and lifetime fitness, without permanently removing individuals from the population or removing body parts. Possible DNA sources for insects include frass, exuviae, and wing and leg clippings. However, these are not feasible approaches for organisms that cannot be removed from their natural environment for long periods or when adverse effects of tissue removal must be avoided. This study evaluated the impacts and efficacy of extracting haemolymph from a defensive secretion to obtain DNA for amplification of microsatellites using a nondestructive technique. A secretion containing haemolymph was obtained from Bolitotherus cornutus (the forked fungus beetle) by perturbation of the defensive gland with a capillary tube. A laboratory experiment demonstrated that the sampling methodology had no impact on mortality, reproductive success or gland expression. To evaluate the quality of DNA obtained in natural samples, haemolymph was collected from 187 individuals in the field and successfully genotyped at nine microsatellite loci for 95.7% of samples. These results indicate that haemolymph‐rich defensive secretions contain DNA and can be sampled without negative impacts on the health or fitness of individual insects.

No evidence for adaptation to local rhizobial mutualists in the legume Medicago lupulina

Abstract Local adaptation is a common but not ubiquitous feature of species interactions, and understanding the circumstances under which it evolves illuminates the factors that influence adaptive population divergence. Antagonistic species interactions dominate the local adaptation literature relative to mutualistic ones, preventing an overall assessment of adaptation within interspecific interactions. Here, we tested whether the legume Medicago lupulina is adapted to the locally abundant species of mutualistic nitrogen‐fixing rhizobial bacteria that vary in frequency across its eastern North American range. We reciprocally inoculated northern and southern M. lupulina genotypes with the northern (Ensifer medicae) or southern bacterium (E. meliloti) in a greenhouse experiment. Despite producing different numbers of root nodules (the structures in which the plants house the bacteria), neither northern nor southern plants produced more seeds, flowered earlier, or were more likely to flower when inoculated with their local rhizobia. We then used a pre‐existing dataset to perform a genome scan for loci that showed elevated differentiation between field‐collected plants that hosted different bacteria. None of the loci we identified belonged to the well‐characterized suite of legume–rhizobia symbiosis genes, suggesting that the rhizobia do not drive genetic divergence between M. lupulina populations. Our results demonstrate that symbiont local adaptation has not evolved in this mutualism despite large‐scale geographic variation in the identity of the interacting species.

Geographically structured genetic variation in the Medicago lupulina – Ensifer mutualism

Gene flow between genetically differentiated populations can maintain variation in species interactions, especially when population structure is congruent between interacting species. However, large‐scale empirical comparisons of the population structure of interacting species are rare, particularly in positive interspecific interactions (mutualisms). One agriculturally and ecologically important mutualism is the partnership between legume plants and rhizobia. Through characterizing and comparing the population genomic structure of the legume Medicago lupulina and two rhizobial species (Ensifer medicae and E. meliloti), we explored the spatial scale of population differentiation between interacting partners in their introduced range in North America. We found high proportions of E. meliloti in southeastern populations and high proportions of E. medicae in northwestern populations. Medicago lupulina and the Ensifer genus showed similar patterns of spatial genetic structure (isolation by distance). However, we detected no evidence of isolation by distance or population structure within either species of bacteria. Genome‐wide nucleotide diversity within each of the two Ensifer species was low, suggesting limited introduction of strains, founder events, or severe bottlenecks. Our results suggest that there is potential for geographically structured coevolution between M. lupulina and the Ensifer genus, but not between M. lupulina and either Ensifer species.

Surprisingly little population genetic structure in a fungus‐associated beetle despite its exploitation of multiple hosts

In heterogeneous environments, landscape features directly affect the structure of genetic variation among populations by functioning as barriers to gene flow. Resource-associated population genetic structure, in which populations that use different resources (e.g., host plants) are genetically distinct, is a well-studied example of how environmental heterogeneity structures populations. However, the pattern that emerges in a given landscape should depend on its particular combination of resources. If resources constitute barriers to gene flow, population differentiation should be lowest in homogeneous landscapes, and highest where resources exist in equal proportions. In this study, we tested whether host community diversity affects population genetic structure in a beetle (Bolitotherus cornutus) that exploits three sympatric host fungi. We collected B. cornutus from plots containing the three host fungi in different proportions and quantified population genetic structure in each plot using a panel of microsatellite loci. We found no relationship between host community diversity and population differentiation in this species; however, we also found no evidence of resource-associated differentiation, suggesting that host fungi are not substantial barriers to gene flow. Moreover, we detected no genetic differentiation among B. cornutus populations separated by several kilometers, even though a previous study demonstrated moderate genetic structure on the scale of a few hundred meters. Although we found no effect of community diversity on population genetic structure in this study, the role of host communities in the structuring of genetic variation in heterogeneous landscapes should be further explored in a species that exhibits resource-associated population genetic structure.

Combining phenotypic and genomic approaches reveals no evidence for adaptation to the local mutualist in Medicago lupulina

Local adaptation is a common but not ubiquitous feature of species interactions, and understanding the circumstances under which it evolves illuminates the factors that influence adaptive population divergence. Antagonistic species interactions dominate the local adaptation literature relative to mutualistic ones, preventing an overall assessment of adaptation within interspecific interactions. Here, we tested whether the legume Medicago lupulina is adapted to the locally abundant species of mutualistic nitrogen-fixing bacteria (“rhizobia”), which vary in frequency across its eastern North American range. We reciprocally inoculated northern and southern M. lupulina genotypes with the northern (Ensifer medicae) or southern bacterium (E. meliloti) in a greenhouse experiment. Neither northern nor southern plants produced more seed flowered earlier, or were more likely to flower when inoculated with their local rhizobium species, although plants produced more root nodules (the structures that house the bacteria) wit their local rhizobia. We used a pre-existing dataset to perform a genome scan for loci that showed elevated differentiation between field-collected plants that hosted different bacteria. None of the loci we identified belonged to the well-characterized suite of legume-rhizobia symbiosis genes, suggesting that the rhizobia do not drive genetic divergence between M. lupulina populations. Our results demonstrate that symbiont local adaptation is weak in this mutualism despite large-scale geographic variation in the identity of the interacting species.Local adaptation is a common but not ubiquitous feature of species interactions, and understanding the circumstances under which it evolves illuminates the factors that influence adaptive population divergence. Antagonistic species interactions dominate the local adaptation literature relative to mutualistic ones, preventing an overall assessment of adaptation within interspecific interactions. Here, we tested whether the legume Medicago lupulina is locally adapted to two species of mutualistic nitrogen-fixing rhizobial bacteria that vary in frequency across its eastern North American range. We reciprocally inoculated northern and southern M. lupulina genotypes with the northern (Ensifer medicae) or southern bacterium (E. meliloti) in a greenhouse experiment, and performed a genome scan for loci that showed elevated differentiation between field-collected plants that hosted different bacteria. Despite producing different numbers of root nodules (the structures in which the plants house the bacteria), neither northern nor southern plants produced more seeds, flowered earlier, or were more likely to flower when inoculated with their local rhizobia. None of the loci identified in our genomic analysis belonged to the well-characterized suite of legume-rhizobia symbiosis genes, suggesting that the rhizobia do not drive genetic divergence between M. lupulina populations. Our results demonstrate that local adaptation has not evolved in this mutualism despite large-scale geographic variation in the identity of the interacting species.