Insects As Models for Studying the Evolution of Animal Cognition

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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

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 problem solving, spatial learning, associative learn- like social complexity [38]. Although large-scale com-

ing, or a combination? A recent study by Li et al. found parative cognition research is methodologically challeng-

that microglomeruli density in the mushroom bodies was ing, these studies offer unique insight into the evolution

linked with an individual’s ability to learn and retain of cognitive skills.

information, suggesting that neuroanatomy may be asso-

ciated with functional differences in insect cognition [44]. Thus far, we lack comparative analyses that directly

Notably, some apparently complex insect behaviors may measure cognition in multiple insect species. We also

involve little information processing and minimal neural lack comparative work that explicitly examines verte-

investment suggesting there may be multiple evolution- brates and insects within the same framework. Insects

ary pathways to complex cognition [41]. Future work that have great potential for comparative cognition research as

directly links insect neuroanatomy with functional differ- they excel at a range of learning tasks. Honeybees are

ences in cognition will provide insight into whether brain/ capable of impressive spatial learning and navigation,

Current Opinion in Insect Science 2019, 34:117–122 www.sciencedirect.com

Insects and the evolution of animal cognition Simons and Tibbetts 119

bumblebees are able to complete multi-step learning long-term memory, inhibitory control, and motor control.

tasks for food rewards [48], and Polistes wasps are capable If multiple aspects of cognition covary, it suggests that

of learning the individual faces of conspeciﬁcs and tran- insect cognition evolves in a domain-general manner. If

sitive inference [16,49,50]. However, insect researchers aspects of cognition are independent, it supports domain-

have yet to develop standardized cognitive tests that can speciﬁc cognitive evolution [52]. Of course, the hypothe-

be used across insect species to assess a variety of cogni- ses are not mutually exclusive. Domain-speciﬁc and

tive domains. In the future, it will be interesting to test domain general processes may interact to mediate cogni-

multiple insects on similar cognitive tasks to assess tive evolution. Understanding how both processes inter-

whether social and ecological factors are linked with act to inﬂuence cognition is key to predicting how socio-

variation in cognitive performance. For example, are ecological variables inﬂuence the evolution of animal

insects with central-place foraging better spatial learners cognition and whether this is consistent across taxa.

than species without central-place foraging? Are insects

that live in complex societies better at cognitively chal- In insects, we lack large-scale studies that compare per-

lenging tasks like problem-solving or reversal learning formance across many cognitive domains, though there is

than insects that do not live in complex societies? There is evidence for links across two cognitive domains [9].

great potential for future work testing whether social and Bombus that rapidly learn to associate a color with a reward

ecological selective pressures act in similar ways to shape are also quick to reverse this association, suggesting that

cognition across vertebrates and insects. associative learning and reversal learning are linked

[43,56]. There is also some evidence of domain-speciﬁc

Specialized versus generalized cognition cognitive differences between paper wasp species. Polistes

Another major challenge associated with quantifying fuscatus wasps use face recognition to identify individual

intelligence is that intelligence is not one trait. It has conspeciﬁcs during social interactions and excel at learn-

multiple components that may vary independently or in ing unique wasp faces. A close relative, Polistes metricus,

concert [51 ]. One hypothesis is that selection acts does not recognize individual conspeciﬁcs and is unable

simultaneously on multiple aspects of cognition to pro- to learn unique wasp faces. Although the two species

duce domain-general differences in cognition (or general differ in their capacity for face learning, they do not differ

intelligence) [52]. The social and ecological intelligence in other types of visual learning [13]. Therefore, the social

hypotheses in Figure 1 posit that social or ecological context requiring individual face recognition inﬂuences

complexity produce domain-general differences in cog- cognition in a very specialized way rather than favoring

nition. Multiple studies in mammals [52] and birds [18 ] large-scale differences in visual discrimination learning.

support domain general cognitive evolution; some indi- This work provides promising evidence that standardized

viduals excel at multiple cognitive tasks, while other cognitive tests can be used to compare multiple insect

perform poorly on multiple tasks. For example, in wild species. Applying similar methods to additional taxa,

New Zealand robins, performance on six distinct cogni- contexts, and questions may provide insight into the

tive tasks were highly correlated, suggesting that a evolution of insect cognition.

general cognitive factor underpins cognitive perfor-

mance on multiple different types of tasks. [53]. The Factors associated with variation in cognition

alternative is that selection acts independently on the Over the past decades, the question of why some animals

speciﬁc cognitive modules involved in a particular task are more intelligent than others has received much atten-

to produce specialized differences in cognition. There is tion, with data supporting many different hypotheses.

some support for domain-speciﬁc cognitive differences Early work often focused on a single hypothesis in a small

[45]. For example, birds that store and retrieve seeds taxonomic group. However, recent vertebrate studies are

have specialized cognitive differences [54]; they excel at using more sophisticated phylogenetic analyses, large

spatial learning, but are no better at other tasks than non- sample sizes, and testing how multiple variables interact

caching species. Overall, there is evidence that selection to inﬂuence cognition. Most of this work quantiﬁes intel-

acts on vertebrates to produce both domain-speciﬁc and ligence as relative brain size. For example, DeCasien et al.

domain-general cognitive differences, though we still analyzed over 140 species of primates, testing whether

have much to learn about the relative importance of multiple measures of sociality and ecology explain varia-

these processes. tion in brain size [4]. They found that brain size is

predicted by diet rather than sociality, suggesting that

Little is known about whether insect cognition evolves in ecology may play a key role in cognitive evolution. This

domain-general or domain-speciﬁc manner. However study highlights the value of large-scale comparative

some recent work suggests behavioral ﬂexibility in insects analyses that simultaneously test multiple hypotheses.

is linked to domain-general cognition [55]. Testing this

hypothesis requires assessing insect cognition across A relatively small number of comparative analyses have

multiple domains, for example, behavioral ﬂexibility, tested the factors associated with insect neural invest-

associative learning, reversal learning, spatial memory, ment, though the results of these studies have been

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120 Social insects

Figure 1

Current Opinion in Insect Science

Table reviewing hypotheses for the evolution of cognition and support for the hypotheses in vertebrates and insects. Note that hypotheses may be

complementary rather than mutually exclusive. Hypotheses referenced include the Social Brain Hypothesis [17,18 ,19–22], Distributed Cognition

Hypothesis [23,24], Cooperative Breeding Hypothesis [25,26], Cognitive Buffer Hypothesis[27], Relationship Intelligence Hypothesis [28], Ecological

Intelligence Hypothesis [2,4,10,29,30], Predator–Prey Interactions [31 ,32–34], and Mate Choice [35,36].

promising. All three studies focused on mushroom bodies, development in the sweat bee, Megalopta genalis, with

an area of the insect brain associated with sensory bees from social groups having relatively larger mushroom

integration and learning. A 2010 study using sweat bees bodies than solitary bees [19]. The ‘distributed cognition

found intriguing support for the social brain hypothesis. hypothesis’ is the only hypothesis initially developed in

They found that sociality inﬂuenced mushroom body insects. It proposes that large-colony insects will have less

Current Opinion in Insect Science 2019, 34:117–122 www.sciencedirect.com

Insects and the evolution of animal cognition Simons and Tibbetts 121

temporal complexity of chimpanzee food: how cognitive

neural investment than smaller colony insects because

adaptations can counteract the ephemeral nature of ripe fruit.

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evolution of large, elaborate mushroom bodies in

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Conﬂict of interest statement

Australian magpies. Nature 2018, 554:364-367.

Nothing declared. Using wild magpies, the authors demonstrate that birds in larger groups

have higher general intelligence than birds from smaller groups, using four

cognitive tests: inhibitory control, associative learning, reversal learning

Acknowledgement and spatial memory. This study effectively combines ﬁeld techniques with

This material is based in part upon work supported by the National Science measuring cognition.

Foundation under grant number IOS-1557564.

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