Animal personality adds complexity to the processes of adaptive divergence and speciation

Abstract

A variety of behavioural traits are now widely recognized as playing a key role in the evolution 68 of animal populations through natural selection [1][2][3]. Traits such as aggressivity, sociality and 69 boldness (the propensity for taking risks) are well studied for their implications on foraging 70 success, predator avoidance, vulnerability to parasites, breeding success, and life-history 71 strategies in a wide range of taxa (e.g. arthropods, vertebrates, molluscs, sea anemones) [4][5][6][7][8][9]. 72Major advances in our understanding of the role of behaviour in evolution have been recently 73 achieved through studies of behavioural differences at the individual level, and focusing on 74 individual consistency, that is, animal personality [10-12]. Behavioural differences among 75populations are now considered as more than adaptive mean values surrounded by the noise of 76 individual variance and can be studied under different aspects, such as (i) the group level, 77 average values of a given behavioural trait, (ii) the consistent differences between individuals 78 in this trait (personality per se) and (iii) the covariations between this trait and others 79 (behavioural syndromes) [4]. Because of their genetic bases and their effects on fitness, 80 personality and behavioural syndromes are considered to be important drivers of adaptive 81 divergence and speciation [3,13,14]. Considering classical models of speciation [15,16], 82 divergent selection may indeed result in the segregation of behavioural types between different 83 fitness optima. Reproductive isolation (such as selection against intermediate or transgressive 84 hybrids) could then develop as a by-product, which may in turn lead to further divergence [17]. 85Despite the recent conceptual advances about the importance of personality in the processes of 86 adaptive divergence and speciation, empirical studies directly investigating it are still lacking 87[14]. Information is especially lacking regarding the behavioural phenotype of hybrids and 88 their contribution to reproductive isolation [18]. 89 90Here we explore whether behaviour as considered under the three aspects described above 91 (average trait value, consistent differences between individuals and trait covariance) can 92 influence the evolutionary processes of divergence and speciation. First, contrasting ecological 93 conditions can generate different fitness optima that favour the differentiation of populations 94 in the average values of a behavioural response (i.e. "behavioural adjustment", Figure 1a) [19]. 95Second, contrasting environmental variables such as the predictability of a food resource or 96 predation risk can determine the benefit of behavioural consistency over plasticity, thus 97 affecting the level of consistent differences between individuals (i.e. personality per se) [20] -98 defined as behavioural "homogenisation" vs. "diversification" in [19] (Figure 1). Finally, 99(the spawning season of SB charr encompassing the one of PL charr) and these two morphs 126 appear t...