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Learning is central to our understanding of how behaviour is shaped by the environment. A key open question is whether learning across contexts evolves as an integrated process, or whether learning in each context is free to evolve separately. Here, we measured learning in two sensory contexts in multiple genotypes and both sexes of two closely related, but ecologically divergent, species of fruit flies, Drosophila simulans and Drosophila sechellia. These species are morphologically very similar but differ dramatically in ecology and population biology. We tested how flies from each genotype, sex and species responded to and learned about different gustatory and visual cues. This approach allowed us to test whether species differences in learning were independent or correlated across contexts. Surprisingly, we found no evidence that D. simulans learned in any of our treatments. In contrast, D. sechellia learned to avoid gustatory stimuli that were paired with an aversive stimulus, as predicted, but unexpectedly learned to approach visual stimuli that were paired with the aversive stimulus. At the genotype level, genotypes, but not species, differed in their naïve responses to stimuli, but genotypes did not differ in learning in either species. Our results demonstrate that D. sechellia indeed differs from D. simulans in both learning contexts, but in a stimulus-dependent way. We suggest that studies of additional species or population pairs that employ this framework will be critical for evaluating the dimensionality of learning and its evolution. 

Social behaviors can be influenced by the genotypes of interacting individuals through indirect genetic effects (IGEs) and can also display developmental plasticity. We investigated how develop- mental IGEs, which describe the effects of a prior social partner’s geno- type on later behavior, can influence aggression in male Drosophila melanogaster. We predicted that developmental IGEs cannot be esti- mated by simply extending the effects of contextual IGEs over time and instead have their own unique effects on behavior. On day 1 of the ex- periment, we measured aggressive behavior in 15 genotypic pairings (n p 600 males). On day 2, each of the males was paired with a new opponent, and aggressive behavior was again measured. We found con- textual IGEs on day 1 of the experiment and developmental IGEs on day 2 of the experiment: the influence of the day 1 partner’s genotype on the focal individual’s day 2 behavior depended on the genotypic iden- tity of both the day 1 partner and the focal male. Importantly, the devel- opmental IGEs in our system produced fundamentally different dynam- ics than the contextual IGEs, as the presence of IGEs was altered over time. These findings represent some of the first empirical evidence dem- onstrating developmental IGEs, a first step toward incorporating de- velopmental IGEs into our understanding of behavioral evolution. 

Abstract Mixed-species groups describe active associations among individuals of 2 or more species at the same trophic level. Mixed-species groups are important to key ecological and evolutionary processes such as competition and predation, and research that ignores the presence of other species risks ignoring a key aspect of the environment in which social behavior is expressed and selected. Despite the defining emphasis of active formation for mixed-species groups, surprisingly little is known about the mechanisms by which mixed-species groups form. Furthermore, insects have been almost completely ignored in the study of mixed-species groups, despite their taxonomic importance and relative prominence in the study of single-species groups. Here, we measured group formation processes in Drosophila melanogaster and its sister species, Drosophila simulans. Each species was studied alone, and together, and one population of D. melanogaster was also studied both alone and with another, phenotypically distinct D. melanogaster population, in a nested-factorial design. This approach differs from typical methods of studying mixed-species groups in that we could quantitatively compare group formation between single-population, mixed-population, and mixed-species treatments. Surprisingly, we found no differences between treatments in the number, size, or composition of groups that formed, suggesting that single- and mixed-species groups form through similar mechanisms of active attraction. However, we found that mixed-species groups showed elevated interspecies male–male interactions, relative to interpopulation or intergenotype interactions in single-species groups. Our findings expand the conceptual and taxonomic study of mixed-species groups while raising new questions about the mechanisms of group formation broadly.