ALBERT

Description: In their recent review, Bailey et al. (2017) make the compelling case that indirect genetic effects (IGEs) should be more widely incorporated into behavioral ecology research. IGEs occur whenever the trait of one individual is affected by the genotype of another “interacting” individual, usually via one or more “social cues.” IGEs create an additional source of heritable variation that can influence an individual’s trait expression above and beyond any direct contributions of its genotype (direct genetic effect [DGE]) and the environment ( Lynch and Walsh 1998 ). When conspecifics interact, as is the case for behavioral interactions, they make up part of an individual’s “social environment” and because these interacting partners are themselves genetically variable, additional heritable variation can be generated. So why does this matter? A key outcome of IGEs is that traits affected by them can evolve not only due to direct genetic variation but also due to evolution of the social environment itself ( Wolf et al. 1998 ).

Description: Behavior is rapidly flexible and highly context-dependent, which poses obvious challenges to researchers attempting to dissect its causes. However, over a century of unresolved debate has also focused on whether the very flexibility and context-dependence of behavior lends it a unique role in the evolutionary origins and patterns of diversity in the Animal Kingdom. Here, we propose that both challenges can benefit from studying how indirect genetic effects (IGEs: the effects of genes expressed in one individual on traits in another individual) shape behavioral phenotypes. We provide a sketch of the theoretical framework that grounds IGEs in behavioral ecology research and focus on recent advances made from studies of IGEs in areas of behavioral ecology such as sexual selection, sexual conflict, social dominance, and parent–offspring interactions. There is mounting evidence that IGEs have important influences on behavioral phenotypes associated with these processes, such as sexual signals and preferences and behaviors which function to manipulate interacting partners. IGEs can also influence both responses to selection and selection itself, and considering IGEs refines evolutionary predictions and provides new perspectives on the origins of seemingly perplexing behavioral traits. A key unresolved question, but one that has dominated the behavioral sciences for over a century, is whether behavior is more likely than other types of traits to contribute to evolutionary change and diversification. We advocate taking advantage of an IGE approach to outline falsifiable hypotheses and a general methodology to rigorously test this frequently proposed, yet still contentious, special role of behavior in evolution.

Description: The notion that behavioral traits “must often take the lead in evolution” because they are “especially plastic” ( West-Eberhard 2003 ) sits somewhat uncomfortably with standard quantitative genetic theory. Under simple models, plasticity actually slows evolution: more plastic traits have greater variance, reduced heritability and so lowered expected selection response. Here, Bailey et al. (2017) highlight the tantalizing possibility that indirect genetic effects (IGEs) could reconcile these contrasting positions. They provide a neat structured list of questions to guide empirical efforts, effectively asking:

Description: The key proposal in Bailey et al. (2018) is that evolutionary processes may be misinterpreted if indirect genetic effects (IGEs) are not taken into consideration. Further, that such processes are a fundamental part of behavior and thus the genetic analysis of behavior and its evolution must take into account IGEs. The authors present a very convincing case for this proposal both from theoretical argument and empirical evidence.

Description: There is growing evidence for consistent among-individual variation in individual sociability (e.g., tendency to be sociable) in a number of species. However, sexes often differ in their social behaviors, as well as the selection pressures which they experience. This may translate into differences in repeatability of sociability, although this has not yet been tested. Here, we investigated whether eastern water dragons ( Intellegama leseurii ) exhibited evidence of consistent among-individual variation (i.e., repeatability) in 4 different measurements of sociability. Specifically, we measured sociability in 4 ways (degree, centrality, proportion of time spent being social, and number of preferences), and tested whether there was evidence for sex differences in the repeatability of these sociability measurements, or whether observed levels of repeatability could be explained by a stable social environment. Our findings provide new evidence for sex differences in social personality: we found that males were significantly repeatable in 3 of 4 sociability measurements (degree, centrality, and proportion of time spent being social), whereas females were not. Further, we found that these differences were not a result of differences in the dynamics of the social environment. We discuss our findings in the context of sexual selection, as well as sex differences in the evolutionary drivers of social behavior.

Description: When foraging in their natural environment, many animals readily complement their personal knowledge with additional social information. To balance the costs and benefits of copying others, animals have to discern situations in which it is more advantageous to use social rather than personal information. Here, we used foraging bumblebees ( Bombus terrestris ) in a controlled laboratory setting and showed that the difficulty of a foraging task affects how the bees weight the 2 types of information. We used artificial flowers to devise easy and difficult discriminatory tasks, and tested the influence of floral and social cues on decision making. When facing an easy discrimination task, foraging bees were likely to rely on personal information and were only marginally affected by social information. By contrast, they prioritized social over personal information when flower discrimination was difficult and therefore the probability of making errors was higher. In summary, bees are able to use social and personal information to optimize foraging decisions in a flexible way.

Description: We propose that indirect genetic effects (IGEs) represent an appealing way to dissect the genetics and evolutionary dynamics of complex phenotypes studied in behavioral ecology. IGEs are complementary to inclusive fitness approaches, but as Kruuk and Wilson (2018) observe, are distinct because they do not require assumptions about relatedness (see also McGlothlin et al. 2014 and McDonald et al. 2017 ). Thus, IGEs open up the opportunity to study any social interaction and any trait expressed in a social interaction (See Roff 2018 ). These features of IGEs have enabled behavioral ecologists to study behavior from a slightly different perspective, as an evolutionary feedback process that links individuals and their environments through genes.

Description: By definition, teaching is both cooperative and costly and so we appreciate Cordony’s (2017) commentary in this spirit. We also agree that the cost of teaching in the superb fairy-wren ( Malurus cyaneus ) system can and should be more fully explored. Kleindorfer, Hoi, et al. (2014) quantified a cost of incubation calling ( Colombelli-Négrel et al. 2012 ) to fairy-wren mothers through the detection of higher egg predation at nests with more incubation calls. The commentary raises 2 main concerns: that 1) Kleindorfer, Hoi, et al. (2014) misinterpreted the operational definition of cost in animal teaching by Caro and Hauser (1992) and its operational interpretation by Thornton and Raihani (2010) , because 2) nest predation is neither an immediate nor a personal cost to the mother.

Description: Although numerous aquatic and terrestrial species adorn their surface with items secured from their surroundings, termed decorating, the physical and environmental factors that drive this behavior are often unclear. One of the best-known examples of this phenomenon are the decorator crabs (Majoidea), with almost 75% of species known to decorate. Here, we examined patterns of decorating in a coral reef-associated majoid, Camposcia retusa , to identify what factors determine patterns of, and investment in, decorating. Observations of natural decoration patterns indicate this species primarily decorate with sponges, fleshy and filamentous algae, and detritus. Decorations were primarily distributed on the carapace and hind walking legs which may reflect exoskeleton morphology. However, decoration cover did not decline with size, as is observed in some other majoid species, suggesting the factors driving decoration investment remain consistent throughout growth stages. From behavioral experiments, we determined that nonuniform decorating is a result of active selection, with crabs preferentially decorating their hind legs and carapace, with only small items placed on the carapace. Decorating in C. retusa appears to function primarily as an antipredator response, with crabs decorating at higher rates when access to shelter is limited. This study is the first to quantify the decorating habits of C. retusa and suggests that behaviorally-mediated decorating has a primary antipredator function. This study also highlights the value of manipulative behavioral experiments as a tool for assessing the behavioral mechanisms that drive decorating in animals.

Description: Pathogens are ubiquitous in nature and typically entail major fitness costs in their hosts. These costs can be particularly important when individuals exhibit poor immune defenses, as it is often the case during early developmental stages. Hence, selection should favor parental strategies limiting the risks of pathogen exposure and infection in their offspring. In this study, we investigated 1) whether females of the European earwig Forficula auricularia avoid areas contaminated with spores of the entomopathogenic fungus Metarhizium brunneum prior to and at egg laying, as well as 2) whether spore presence entails an increase in females’ investment into both pre-hatching forms of care and clutch quantity and quality. Our results first show that females did not avoid contaminated areas prior to and at egg laying. However, females returned to their eggs faster in presence of living spores compared to UV-killed or no spores. They were also more likely to construct a nest when in presence of both living and UV-killed spores (but only in one studied population). Finally, we found that spore presence did not influence maternal investment into egg grooming, egg gathering and egg defense, as well as into clutch quantity and quality. Overall, our results demonstrate that earwig females do not avoid contaminated environments, but could mitigate the associated costs of pathogen exposure by adjusting their level of egg care. These findings emphasize the importance of pathogens in the evolution of pre-hatching parental care and, more generally, in the emergence and maintenance of family life in nature.