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Insects As Models for Studying the Evolution of Animal Cognition

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Insects As Models for Studying the Evolution of Animal Cognition Available online at www.sciencedirect.com ScienceDirect Insects as models for studying the evolution of animal cognition Meagan Simons and Elizabeth Tibbetts Research on the evolution of cognition has long centered on finding stronger support for ecological selection pressures vertebrates. Current research indicates that both complex [4,5], and other studies finding stronger support for social social behavior and ecology influence the evolution of selection pressures [6]. In recent years, there has been a vertebrate cognition. Insects provide a powerful and growing appreciation that social and ecological factors often underappreciated model system for research on cognitive work together to influence the evolution of cognition [7 ]. evolution because they are a large group with multiple Multiple selective forces, and non-selective constraints evolutionary transitions to complex social behavior as well as interact to shape cognitive evolution [6,7 ]. extensive ecological variation. Here, we integrate current research on cognitive evolution in vertebrates and insects. We In this review, we will integrate research on vertebrate specifically highlight recent advances in vertebrate research and insect cognition and highlight opportunities for that are applicable to insects. We focus on two key topics: future research. Cognition is the ability to acquire, pro- 1) The challenges of quantifying cognition 2) What factors cess, store, and act on information [8]. Vertebrate studies contribute to the evolution of cognition? Applying methods like often use ‘intelligence’ interchangeably with ‘cognition’ comparative analysis and behavioral cognition measurement to [9]. We use both terms in this review because using insects are likely to provide key insight into the evolution of similar terminology facilitates research integration across animal minds. vertebrates and insects. As described in more detail in the section ‘Challenges of Quantifying Cognition’, quantify- Address ing and comparing cognition across taxa are challenging University of Michigan, 1105 N. University Ave., Ann Arbor, MI 48104, because it is difficult to fully capture cognitive variation United States with a single variable [10]. Nevertheless, comparative Corresponding author: Tibbetts, Elizabeth ([email protected]) analyses provide a powerful method for studying cogni- tive evolution [11]. There is much potential for future work combining neuroanatomical and behavioral metrics Current Opinion in Insect Science 2019, 34:117–122 to assess cognition in diverse insects. This review comes from a themed issue on Social insects Edited by Patrick Abbot and Sarah Kocher Thus far, the vast majority of theoretical and empirical work on cognitive evolution has focused on vertebrates. As a result, insect and other invertebrate researchers will benefit by using the conceptual framework developed by https://doi.org/10.1016/j.cois.2019.05.009 vertebrate researchers to understand variation in insect 2214-5745/ã 2019 Elsevier Inc. All rights reserved. cognition. In addition, the broader field of cognitive evolution will benefit from incorporating insect research because insects provide an important comparative per- spective. Insects and vertebrates have independently evolved complex behaviors such as cooperation, cen- tral-place foraging, navigation, and complex communica- Introduction tion with conspecifics [12,13]. Insects and vertebrate There is enormous variation in cognitive complexity and brains also have distinct neural structures and diverged brain size across species. Many explanations have been approximately 600 mya [14]. Identifying similarities and proposed for the variation in cognition. The two best- differences between how insect and vertebrate cognition known hypotheses are the ‘ecological intelligence’ and co-evolves with behavior will clarify how selection has ‘social intelligence’ hypotheses. The ‘ecological intelli- shaped cognition in diverse taxa, the generality of hypoth- gence hypothesis’ proposes that the need to find and eses developed for vertebrates, as well as how cognitive process food plays a key role in the evolution of enhanced evolution differs across distinct neural structures. cognition [1,2]. The ‘social intelligence hypothesis’ pro- Although there has been some notable research on the poses that large brains and enhanced cognition are favored evolution of brain size and neuroanatomy in insects in species that live in complex societies because individuals [15,16], we still know relatively little about the evolution with superior cognitive capacity are better able to track of insect cognition and many key hypotheses have not many social relationships and respond appropriately [3]. been tested in insects or other invertebrates. Here, we Both hypotheses have received support, with some studies will review existing research on cognitive evolution in www.sciencedirect.com Current Opinion in Insect Science 2019, 34:117–122 118 Social insects insects and describe opportunities for future research. We behavior relationships are broadly applicable across taxo- will focus on two key aspects of cognitive evolution: nomic groups or whether there are multiple routes to 1) Challenges of quantifying cognition 2) What factors complex behavior, some of which require more informa- contribute to the evolution of cognition? tion processing than others. Challenges of quantifying cognition Cognitive test battery Brain behavior relationships An alternative method for assessing intelligence is mea- A major challenge associated with studying the evolution suring intelligence directly with a battery of cognitive of animal cognition is how to quantify cognition. Histori- tests rather than relying on proxies like relative brain size cally, brain size was used as the key metric for measuring [9,18 ,45,46 ]. The major challenge associated with mea- intelligence [37]. Whole brain size is relatively easy to suring cognition directly is that it is logistically difficult to measure and there is some correlative evidence that design and implement appropriate cognitive tests that can vertebrates with larger brain to body size ratios are be used across many taxonomic groups. As a result, more intelligent than those with smaller brain to body cognitive test batteries have only been attempted in a size ratios [38,39]. Although relative brain size studies small number of mammal [27] and bird [18 ] species. One have been influential, relative brain size is an overbroad impressive example is Ashton et al. work on individual and inaccurate measure of cognitive ability [40,41]. As a cognitive performance in wild Australian Magpies [18 ]. result, most current research uses more specific neuroan- Wild birds were tested on four different types of tasks: atomical metrics as a proxy for intelligence [15]. Many inhibitory control, associative learning, reversal learning, studies measure variation in the size of specific parts of and spatial memory. They found that performance on all the brain to which a particular function can be ascribed four tests was correlated, suggesting that some birds have [15,19]. For example, analysis of social intelligence focus higher general intelligence than other birds. Further, on brain areas such as the isocortex, cerebellum, and the individuals from larger groups performed better than forebrain (vertebrates) or mushroom bodies and the cen- those from small groups, suggesting that living in large, tral complex (insects) [19,42]. These metrics are more socially complex groups may promote general intelli- informative than whole brain size as they incorporate gence. The results indicate that living in social groups more specific analyses of selective pressure acting on may shape general cognitive development and evolution neural function. However, it is still difficult to attribute within species. This work also highlights the value of field neuroanatomical variation to specific behavioral traits experiments where multiple aspects of cognition are because many areas of the brain regulate diverse measured. behavior. For example, bird forebrain volume has been correlated with many behaviors, including innovation Given the challenges of measuring cognition across frequency, invasion success, social complexity, food multiple species, there have been few interspecific anal- hoarding, and bower complexity [40]. It is not clear yses that directly measure vertebrate cognition with how different behaviors interact to influence neural behavioral tests. In one notable study, MacLean et al. investment specifically, or whether or not neural invest- assessed the cognitive performance of 36 mammal and ment in specific brain regions correlates to general bird species with a problem-solving task that measured intelligence. self-control [47]. They found that diet but not social group size was a strong predictor of species differences in In insects, both whole brain volume and specific neuro- self-control. This work provides intriguing support for anatomical metrics have been used in comparative ecological rather than social factors influencing the evo- analyses [15,19,20]. However, unlike vertebrates, neuro- lution of a cognitive skill. Subsequently, Benson-Amram anatomical metrics linking functional differences in et al. measured problem solving in 39 mammalian carni- cognition are still relatively understudied [43]. For exam- vore species, finding that problem solving was linked ple, are relatively larger mushroom bodies linked with with relative brain size, but not socioecological variables better
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