Vincent A. Formica

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.

Examining the social landscapes of alternative reproductive strategies

Social environments are inherently dynamic, often changing depending on the frequency and outcomes of conspecific interactions – they can be simultaneously the targets and agents of selection. Understanding how organisms settle in heterogeneous social environments and the effects this has on reproductive success is vital to our understanding of the selective forces at work in wild populations. From an intensive behavioural and ecological study of territoriality in the polymorphic white‐throated sparrow (Zonotrichia albicollis), we demonstrate that males of the two morphs inhabit social niches that correspond to their respective alternative reproductive strategies. By integrating molecular ecology and Geographic Information Systems, we generated continuous, socio‐spatial models of local conspecific density and cuckoldry risk. Our results suggest that the morphs segregate their territories based on socio‐spatial variables, creating a heterogeneous social landscape that matches each behavioural phenotype with a favourable social environment. Specifically, the monogamous tan males tended to settle in low‐density areas that were also low for cuckoldry risk, while the opposite was true for the promiscuous white males. This pattern of socio‐spatial heterogeneity, combined with the social niche partitioning we observed, might act as a social niche polymorphism, and play an important role in maintenance of the alternative reproductive strategies of the white‐throated sparrow. Socio‐spatial factors, similar to those observed in the white‐throated sparrow, may play important roles in the evolution of mating systems in other species, even those with more continuous or cryptic variation.

Differences in Defensive Volatiles of the Forked Fungus Beetle, Bolitotherus cornutus, Living on Two Species of Fungus

Forked fungus beetles, Bolitotherus cornutus, feed, mate, and live on the brackets of several species of shelf fungus that grow on decaying logs. In response to the specific threat stimulus of mammalian breath, B. cornutus beetles produce a volatile defensive secretion. We tested beetles collected from different host fungi to determine whether defensive secretion blends varied with host type. Using solid phase microextraction and gas chromatography-mass spectrometry, we detected large amounts of the alkylated benzoquinones, methyl-p-benzoquinone (toluquinone) and ethyl-p-benzoquinone, and smaller quantities of p-benzoquinone, 3-methylphenol (m-cresol), 3-ethylphenol, 2-methylhydroquinone, and 2-ethylhydroquinone in secretions. Volatile composition did not differ between male and female beetles. Secretions did differ between beetles collected from two species of fungus, Ganoderma applanatum and Fomes fomentarius, with the relative amount of p-benzoquinone secreted being the most important factor. Other relationships among the volatile components are discussed.

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.

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.

Morphological Correlates of a Combat Performance Trait in the Forked Fungus Beetle, Bolitotherus cornutus

Combat traits are thought to have arisen due to intense male-male competition for access to females. While large and elaborate weapons used in attacking other males have often been the focus of sexual selection studies, defensive traits (both morphological and performance) have received less attention. However, if defensive traits help males restrict access to females, their role in the process of sexual selection could also be important. Here we examine the morphological correlates of grip strength, a defensive combat trait involved in mate guarding, in the tenebrionid beetle Bolitotherus cornutus. We found that grip strength was repeatable and differed between the sexes. However, these differences in performance were largely explained by body size and a non-additive interaction between size and leg length that differed between males and females. Our results suggest that leg size and body size interact as part of an integrated suite of defensive combat traits.

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.

Consistent patterns of male mate preference in the laboratory and field

Mate preference by males is a widely observed phenomenon; however, it is not well understood how these preferences are expressed in wild populations. Most studies that describe the expression of male mate preference in the wild tend to observe assortative mating, where higher quality males express a strong preference for high quality females while low quality males express either no preference or a preference for low quality females. We examined male mate preference in Bolitotherus cornutus, the forked fungus beetle, a system that exhibits male–male combat and protracted male courtship. We conducted no-choice trials in the laboratory and monitored male courtship in a wild population. In the laboratory, we found a strong preference for larger, more fecund females across all sizes of males. Results from the field were similar to those in the lab; larger females were courted more often, and there was no relationship between the size of a male and the mean size of females he courted (i.e., no assortative mating). This study documents an unusual pattern of expression of male mate preference in the wild and suggests that mate preference by males may be underappreciated in species with intense male–male competition and non-assortative mating.Significance statementWhile males of many species express a preference for high-quality females, their preferences can change in complex social situations such as those in wild populations, often resulting in pairing for quality. However, recent mathematical theory suggests that male preference could evolve in a variety of social contexts. We studied the mate preferences of male forked fungus beetles in the laboratory and a wild population. In the lab, males of all sizes preferred larger females. In the complex social environment of a wild population, males still preferred larger females even though there was a strong male-male competition. There was no pairing for quality as often observed in other species. These results suggest that male mate preferences may evolve in a variety of systems not just those with flexible preferences and pairing for quality.