Heritability and correlations among learning and inhibitory control traits

Abstract

To understand the evolution of cognitive abilities, we need to understand both how selection acts upon them and their genetic (co)variance structure. Recent work suggests that there are fitness consequences for free-living individuals with particular cognitive abilities. However, our current understanding of the heritability of these abilities is restricted to domesticated species subjected to artificial selection. We investigated genetic variance for, and genetic correlations among four cognitive abilities: inhibitory control, visual and spatial discrimination, and spatial ability, measured on >450 pheasants, Phasianus colchicus, over four generations. Pheasants were reared in captivity but bred from adults that lived in the wild and hence, were subject to selection on survival. Pheasant chicks are precocial and were reared without parents, enabling us to standardize environmental and parental care effects. We constructed a pedigree based on 15 microsatellite loci and implemented animal models to estimate heritability. We found moderate heritabilities for discrimination learning and inhibitory control (h2 = 0.17–0.23) but heritability for spatial ability was low (h2 = 0.09). Genetic correlations among-traits were largely positive but characterized by high uncertainty and were not statistically significant. Principle component analysis of the genetic correlation matrix estimate revealed a leading component that explained 69% of the variation, broadly in line with expectations under a general intelligence model of cognition. However, this pattern was not apparent in the phenotypic correlation structure which was more consistent with a modular view of animal cognition. Our findings highlight that the expression of cognitive traits is influenced by environmental factors which masks the underlying genetic structure.

How general is cognitive ability in non-human animals? A meta-analytical and multi-level reanalysis approach

“…Most of these genetic and among-individual correlations were weak (e.g. [21]), while some were negative (e.g. [61,62]), similar to the negative among-litter correlation we found between passive avoidance and odour discrimination.…”

“…The individual gambit can be avoided by using multivariate mixed-effect models (MMMs) to partition (co)variance patterns at the among-versus within-individual levels [17,19]. MMMs are particularly useful when investigating trade-offs [20] or multivariate correlation structures such as in the study of general intelligence [21]. However, the application of this framework to the study of cognitive traits remains scarce, mostly because (i) studies used single measurements per individual and/or (ii) studies elected to reduce dimensionality using factoranalytical procedures to convert cognitive performance across tasks to a single general factor.…”

“…To date, only a few animal studies have studied the genetic architecture of cognitive abilities (e.g. [21]). Instead, most studies of g in animals take the 'phenotypic gambit', which assumes that the strength and direction of selection on observed phenotypes is sufficient to predict evolutionary trajectories [22][23][24].…”

No evidence for cross-contextual consistency in spatial learning and behavioural flexibility in a passerine

“…On the other, it remains unclear whether selection on individual variation in cognitive traits will result in a meaningful response (Shaw & Schmelz, 2017). One reason for this uncertainty over the evolutionary consequences of selection on cognition is that estimates of heritability are almost entirely lacking from natural populations (Langley et al, 2020;Quinn et al, 2016;reviewed in Croston et al, 2015), partly because generating reliable estimates of heritability demand large pedigrees (Quinn et al, 2006), and instead most researchers are forced to accept the phenotypic gambit, i.e., to assume that if a trait is repeatable, it is likely to be heritable, or that if two traits are phenotypically correlated, they are also genetically correlated (but see Quinn et al, 2016).…”

Spatial cognitive ability is associated with transitory movement speed but not straightness during the early stages of exploration

“…These mixed groups meant that there were likely to be few full siblings, reducing any potential clutch effects on either cognition or movement behaviour. Actual relatedness between individuals used in this study was calculated from blood samples for another study [ 43 ] (electronic supplementary material, Appendix S1). Once laying was completed, we released the adult birds at a location 6.9 km away from the study site.…”