Individual animals frequently exhibit repeatable differences from other members of their population, differences now commonly referred to as ‘animal personality’. Personality differences can arise, for example, from differences in permanent environmental effects―including parental and epigenetic contributors―and the effect of additive genetic variation. Although several studies have evaluated the heritability of behavior, less is known about general patterns of heritability and additive genetic variation in animal personality. As overall variation in behavior includes both the among-individual differences that reflect different personalities and temporary environmental effects, it is possible for personality to be largely genetically influenced even when heritability of behavior per se is quite low.
The relative contribution of additive genetic variation to personality variation can be estimated whenever both repeatability and heritability are estimated for the same data.
Using published estimates to address this issue, we found that ~52% of animal personality variation was attributable to additive genetic variation. Thus, while the heritability of behavior is often moderate or low, the heritability of personality is much higher.
Our results therefore (1) demonstrate that genetic differences are likely to be a major contributor to variation in animal personality and (2) support the phenotypic gambit: that evolutionary inferences drawn from repeatability estimates may often be justified.
…To test the contribution of additive genetic variance to personality variation, we obtained estimates of τ and h2 from the literature in 2 ways. First, we used data sources previously collected by et al 2002 in their review of heritabilities of behavior. This previous search reviewed the behavioral literature to the end of the year 2000 and yielded 70 articles. Second, we conducted a search of 12 leading behavioral ecology, behavioral genetics and evolutionary ecology journals. The journals we included in our search were The American Naturalist, Evolution, Ecology, Behavioral Ecology, Animal behavior, Behavior Genetics, Heredity, Behaviour, Ethology, Journal of Evolutionary Biology, Journal of Animal Ecology and Proceedings of the Royal SocietyB. For behavioral journals, we used the keywords ‘heritability’ and ‘heritab✱’, while for evolutionary ecology journals we used the keywords ‘heritab✱ AND behav✱’ for all articles published in these journals between January 2000 to September 2012. This yielded an additional 236 articles. Of these 306 total articles, only 12 reported both heritability and repeatability [ie. measurement error, which biases downwards to 0] of at least one behavior. The other 294 articles may have reported one parameter or the other, or simply discussed both heritability and repeatability. From these 12 studies―which included 121 pairs of estimates―we extracted all reported estimates of τ and h2, species names, and traits measured. We only included non-human animals in the dataset—thereby excluding one study and 13 pairs of estimates. We also excluded h2 or τ estimates greater than 1 or less than 0,22 which removed 14 pairs of estimates and one article entirely. From the remaining 10 articles and 94 estimates, we excluded all cases in which h2 was estimated as greater than τ. While h2 can be greater than τ under special circumstances,23 a review of available estimates did not suggest these circumstances were met and suggested that these instances were instead a product of estimation error. This screening reduced the dataset to 71 estimates. We removed an additional pair of estimates (ie. one record in the dataset) as they showed up twice in the dataset, once via mid-parent:son and once as mid-parent:mid-offspring (we retained the mid-offspring estimate). These searches and inclusion criteria resulted in a dataset of 70 instances from 10 studies in which h2 and τ were jointly estimated for the same behavior with the same data (electronic supplementary material, Table S1).
Data Analysis: To assess support for both the ‘phenotypic gambit’ as it pertains to behaviors and the degree to which personality variation can be attributed to additive genetic variation, we calculated the ratio of heritability to repeatability for each of the 70 estimates from 10 studies. This ratio, as demonstrated in equations (1.5) and (1.6), is key to both questions. First, as this ratio increases, the phenotypic gambit can be made more reliably. Second, this ratio explicitly estimates the relative contribution of additive genetic variation to personality variation.
To estimate this ratio, we used a linear random-effects model with the study from which estimates were drawn included as a random effect. This model was fitted using restricted estimate maximum likelihood. The intercept of this model provides an estimate of equations (1.5) and (1.6) after controlling for non-independence of studies. We also estimated the 95% confidence interval (CI) around this estimate.
Finally, we qualitatively compared differences in the relative contribution of additive genetic variation to personality variation based on the types of behaviors assayed.
…qualitatively it appears that personality variation in aggression and anti-predator behavior may have a stronger genetic component than for other types of behaviors included in our dataset (Figure 2). These behaviors also tended towards having higher repeatabilities and higher heritabilities (Figure 2).
…As an aside, our discussion of repeatability and heritability variance components (eg. Equations (1.3)–(1.6)) has excluded mention of measurement error as a source, of variation. Measurement error will be present in all studies, but will typically be conflated with VTE, leading to underestimations of repeatability, heritability and the heritability of personality. However, sources of error might occasionally be conflated with Vind, for example when different recording methods or different observers are used on a particular subset of study subjects.