1 How and why are some species so smart? A comment on Rowe & Healy 2 Alex Thornton* 3 4 * 5 Penryn Campus, Treliever Road, Penryn TR10 9FE, UK 6 Address correspondence to A. Thornton. E-mail: alex.thornton@exeter.ac.uk Centre for Ecology and Conservation, Department of Biosciences, University of Exeter, 7 8 Examining how individual cognitive variation relates to fitness holds the promise of 9 providing a richer understanding of how cognitive traits evolve (Thornton and Lukas 2012). 10 However, as Rowe and Healy (2014) point out (see also Thornton, Isden, and Madden 2014 11 in this issue), this endeavour is rife with pitfalls, and requires more psychological rigour than 12 has been employed in most studies to date. I agree wholeheartedly with them that arbitrary 13 “problem-solving” tasks should be abandoned in favour of psychologically-grounded tests 14 targeting specific cognitive mechanisms (Thornton, Isden, and Madden 2014) and hope that 15 future work will heed their advice in designing tests and accounting for non-cognitive 16 influences. Here I want to focus on two additional, interrelated issues: which species should 17 we focus on, and what cognitive mechanisms should we examine? 18 Choices of study species will largely be determined by practical considerations such as the 19 need for an adequate sample size. Abundant, tractable, yet seemingly cognitively 20 unsophisticated model systems may prove useful in developing methods and testing general 21 principles. Such animals have long been a cornerstone of experimental psychology and could 22 be tested in the field to illuminate general principles including trade-offs in cognitive 23 processing (e.g. speed vs. accuracy; Sih and Del Giudice 2012) or between cognition and 24 other traits (e.g. (Mery and Kawecki 2003) in the face of natural selective pressures. I would 25 argue that yet greater insights may be gained by examining the fitness consequences of 26 cognitive variation in animals whose cognitive abilities appear in some way remarkable. 27 Given the costs of investment in neural tissue, what are the fitness benefits that generate 28 selection for these abilities? Food-storing birds provide the paradigmatic example, as there is 29 strong evidence linking the challenges of retrieving stored food with elevated hippocampal 30 volume and long-term memory retention (see Rowe and Healy 2014). Spatial memory tests 31 may offer similar opportunities in other animals, such as female brood parasites, which must 32 remember the locations of potential hosts’ nests (Reboreda, Clayton, and Kacelnik 1996), 33 though the relevant facets of spatial memory are yet to be determined. Here, individual-based 34 studies can help pinpoint which, if any, aspects of spatial memory confer fitness advantages 35 and specify what those advantages may be. 36 37 Arguably, an even greater mystery is the striking performance of some species not only in a 38 single, ecologically predictable cognitive domain, but across domains. For instance, meta- 39 analyses show that some primate species consistently outperform others across different 40 laboratory tasks (Deaner, van Schaik, and Johnson 2006). Among birds, corvids may also 41 exhibit similar cross-context cognitive prowess, with evidence for remarkable abilities in 42 memory, planning, rule learning, inferential reasoning and aspects of physical and social 43 cognition (Seed, Emery, and Clayton 2009). One fruitful avenue of research may be to test 44 the performance of wild individuals across batteries of tasks targeting different cognitive 45 processes (c.f. Isden et al. 2013). While it is difficult to generate straightforward predictions, 46 such work may help elucidate the mechanistic structure of cognition (e.g. the extent to which 47 general mechanisms explain individual performance across different tasks) and understand 48 whether selection acts on cognitive mechanisms as discrete traits or part of an inter-related 49 complex. 50 As Rowe and Healy (2014) remind us, it would be naïve to suppose that individual cognitive 51 performance will necessarily correlate positively with fitness. However, exploring the 52 relationships between suites of cognitive measures and multiple fitness components may help 53 build a picture of the costs and benefits of cognitive traits. We have argued that there is much 54 to be learned from psychometrics, a branch of psychology specifically concerned with 55 quantifying individual cognitive differences (Thornton, Isden, and Madden 2014). In 56 particular, psychometric tests aim to reduce the influence of non-cognitive factors and 57 generate continuous measures of cognitive performance. These tests typically specify clear 58 criteria as to what constitutes a “correct” outcome, but apparent mistakes will also be 59 informative, for example in revealing individual differences in sampling strategies (Seed et 60 al. 2012). By uniting psychometric approaches with conceptual and methodological tools 61 from behavioural ecology, we can start to hone in on trade-offs and understand whether and 62 how selection acts on cognitive variation. 63 64 65 Funding 66 A.T. was supported by a BBSRC David Phillips Fellowship (BB/H021817/1). 67 68 Acknowledgements 69 I am grateful to J. Madden for helpful comments on previous drafts of the paper. 70 71 References 72 Deaner RO, van Schaik CP, Johnson V. 2006. Do some taxa have better domain-general 73 cognition than others ? A meta- analysis of nonhuman primate studies. Evol. Psychol. 4:149– 74 196. 75 Isden J, Panayi C, Dingle C, Madden J. 2013. Performance in cognitive and problem-solving 76 tasks in male spotted bowerbirds does not correlate with mating success. Anim Behav. 86: 77 829-838. 78 Mery F, Kawecki TJ. 2003. A fitness cost of learning ability in Drosophila melanogaster. 79 Proc. R Soc. B 270:2465–2469. 80 Reboreda JC, Clayton NS, Kacelnik A. 1996. Species and sex differences in hippocampus 81 size in parasitic and non-parasitic cowbirds. Neuroreport 7:505–508. 82 Rowe, C, Healy SD 2014 Measuring variation in cognition. Behav. Ecol. In Press. 83 Seed AM, Emery NJ, Clayton NS. 2009. Intelligence in corvids and apes: a case of 84 convergent evolution? Ethology 115:401–420. 85 Seed AM, Seddon E, Greene B, Call J. 2012. Chimpanzee “folk physics”: bringing failures 86 into focus. Phil. Trans. R. Soc. B 367: 2743-2752. 87 Thornton A, Isden J, Madden JR. 2014 Towards wild psychometrics: linking individual 88 cognitive differences to fitness. Behav. Ecol. In press 89 Thornton A, Lukas D. 2012. Individual variation in cognitive performance: developmental 90 and evolutionary perspectives. Phil. Trans. R. Soc. B 367:2773–2783. 91