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 evolution. This idea receives support from comparative studies that link variation in group size or mating systems with cognitive and neuroanatomical differences across species, but findings are contradictory and contentious. 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.

Extended Data Fig. 1. Adult cognitive test battery.

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

Extended Data Fig. 2. Developmental trajectory of cognitive performance.

The developmental trajectory of Australian magpies at 100, 200, and 300 days post-fledging in two cognitive traits: (a) behavioural inhibition (n=48 trials) (b) spatial memory (n=46 trials), and (c) 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 pass the task, or the number of locations searched, so smaller scores indicate better performance.

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

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

Extended Data Fig. 4. Juvenile cognitive test batteries.

Cognitive test batteries presented to individuals at 100 (a-c), 200 (d-f), and 300 (g-i) days post-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). Figure (b) is black because individuals were unable to complete the associative and reversal learning tasks at 100 days post-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 Fig. 5. 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 would swivel when pecked, allowing individuals to search wells for their contents.

Figure 1. The relationship between group size and cognition.

The relationship between group size and cognitive performance in a (a) inhibitory control task, n = 56 individuals, (b) associative learning task, n = 48 individuals, (c) reversal learning task, n = 48 individuals, and (d) spatial memory task, n = 49 individuals. Lines represent best fit. Performance is measured as either the number of trials taken to pass the task, or the number of locations searched, so smaller scores indicate better performance.

Figure 2. The relationship between group size and general cognitive performance.

Individual measures of general cognitive performance derived from principal components analysis. n = 46 individuals.

Figure 3. The relationship between general cognitive performance and group size in juveniles.

The relationship between general cognitive performance and group size at (a) 200 days post-fledging. n=15 individuals, and (b) 300 days post-fledging. n=10 individuals. General cognitive performance could not be computed at 100 days post-fledging.

Figure 4. The relationship between female traits and reproductive success.

The relationship between (a) foraging efficiency and the average number of hatched clutches per female per year, (b) general cognitive performance and the average number of hatched clutches per female per year, (c) general cognitive performance and the average number of fledglings per female per year, and (d) general cognitive performance and the average number of fledglings surviving to independence per female per year. n = 22 individuals.