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Cognitive performance is linked to group size and affects fitness in Australian magpies

Abstract

The social intelligence hypothesis states that the demands of social life drive cognitive evolution1,2,3. This idea receives support from comparative studies that link variation in group size or mating systems with cognitive and neuroanatomical differences across species3,4,5,6,7, but findings are contradictory and contentious8,9,10. To understand the cognitive consequences of sociality, it is also important to investigate social variation within species. Here we show that in wild, cooperatively breeding Australian magpies, individuals that live in large groups show increased cognitive performance, which is linked to increased reproductive success. Individual performance was highly correlated across four cognitive tasks, indicating a ‘general intelligence factor’ that underlies cognitive performance. Repeated cognitive testing of juveniles at different ages showed that the correlation between group size and cognition emerged in early life, suggesting that living in larger groups promotes cognitive development. Furthermore, we found a positive association between the task performance of females and three indicators of reproductive success, thus identifying a selective benefit of greater cognitive performance. Together, these results provide intraspecific evidence that sociality can shape cognitive development and evolution.

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Figure 1: The relationship between group size and cognition.
Figure 2: The relationship between group size and general cognitive performance.
Figure 3: The relationship between general cognitive performance and group size in juveniles.
Figure 4: The relationship between female traits and reproductive success.

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Acknowledgements

We thank E. Russell and the late I. Rowley for access to their life-history records, and for allowing us to continue work on their Guildford magpie population; A. Wolton for help with fieldwork; R. Lymbery for help with statistical analyses; and N. Boogert and A. Young for helpful comments and discussion. This work was funded by an ARC Discovery grant awarded to A.R.R., A.T. and M. B. V. Bell, and a University of Western Australia International Postgraduate Research Scholarship and Endeavour Research Fellowship awarded to B.J.A. A.T. received additional support from a BBSRC David Phillips Fellowship (BB/H021817/1).

Author information

Authors and Affiliations

Authors

Contributions

B.J.A., A.R.R. and A.T. conceived and designed the study. B.J.A. wrote the manuscript. B.J.A. and E.K.E. carried out data collection. All authors discussed results and commented on the manuscript.

Corresponding authors

Correspondence to Benjamin J. Ashton, Amanda R. Ridley or Alex Thornton.

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Competing interests

The authors declare no competing financial interests.

Additional information

Reviewer Information Nature thanks T. Bugnyar and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Figure 1 Adult cognitive test set.

ac, The cognitive test series used to quantify individual variation in inhibitory control (a), associative and reversal learning (b) and spatial memory (c).

Extended Data Figure 2 Developmental trajectory of cognitive performance.

a, b, The developmental trajectory of Australian magpies at 100, 200 and 300 days after fledging for two cognitive traits: behavioural inhibition (a; n = 48 trials) and spatial memory (b; n = 46 trials). c, Developmental trajectory for behavioural inhibition and spatial memory combined (n = 94 trials). Green dots, individuals from small groups (containing 1–7 individuals); blue dots, individuals from large groups (≥8 individuals). Scores are measured as either the number of trials taken to succeed at the task or the number of locations searched, so lower scores indicate better performance.

Source data

Extended Data Figure 3 Frequency distribution of general cognitive performance in relation to group size.

a, b, Frequency distribution of general cognitive performance among individuals in small groups (a; containing <8 individuals, n = 29 individuals) and large groups (b, >8 individuals, n = 17 individuals).

Source data

Extended Data Figure 4 Juvenile cognitive test batteries.

ai, Cognitive test batteries presented to individuals at 100 (ac), 200 (df) and 300 (gi) days after fledging, containing four tasks designed to quantify inhibitory control (a, d, g), associative and reversal learning (b, e, h) and spatial memory (c, f, i). b is shown in black and white, because individuals were unable to complete the associative and reversal learning tasks at 100 days after fledging. Red circles indicate that individuals had to search a different location at each age tested in order to obtain the food reward in the spatial memory task.

Extended Data Figure 5 Example of the lids used in the cognitive tasks.

The lids used in the associative learning, reversal learning and spatial memory tasks. The lids were held firmly in place by elastic bands, and swivelled when pecked, allowing individuals to search wells for their contents.

Extended Data Table 1 Principal component analysis (adults)
Extended Data Table 2 Repeatability of cognitive performance
Extended Data Table 3 Principal component analysis (200 days after fledging)
Extended Data Table 4 Principal component analysis (300 days after fledging)

Supplementary information

Supplementary Information

This file contains Supplementary Results and Discussion, Supplementary References and Supplementary Tables 1-26. (PDF 1175 kb)

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Ashton, B., Ridley, A., Edwards, E. et al. Cognitive performance is linked to group size and affects fitness in Australian magpies. Nature 554, 364–367 (2018). https://doi.org/10.1038/nature25503

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