Abstract
Multilevel selection has rarely been studied in the ecological context of animal populations, in which neighbourhood effects range from competition among territorial neighbours to source-sink effects among local populations. By studying a Dupont’s lark Chersophilus duponti metapopulation, we analyze neighbourhood effects mediated by song repertoires on fitness components at the individual level (life-span) and population level (growth rate). As a sexual/aggressive signal with strong effects on fitness, birdsong creates an opportunity for group selection via neighbour interactions, but may also have population-wide effects by conveying information on habitat suitability to dispersing individuals. Within populations, we found a disruptive pattern of selection at the individual level and an opposite, stabilizing pattern at the group level. Males singing the most complex songs had the longest life-span, but individuals with the poorest repertoires lived longer than ‘average’ males, a finding that likely reflects two male strategies with respect to fitness and sexual trait expression. Individuals from groups with intermediate repertoires had the longest life-span, likely benefitting from conspecific signalling to attract females up to the detrimental spread of competitive interactions in groups with superior vocal skills. Within the metapopulation selection was directional but again followed opposite patterns at the two levels: Populations had the highest growth rate when inhabiting local patches with complex repertoires surrounded by patches with simple repertoires. Here the song may impact metapopulation dynamics by guiding prospecting individuals towards populations advertising habitat quality. Two fitness components linked to viability were therefore influenced by the properties of the group, and birdsong was the target of selection, contributing to linking social/sexual processes at the local scale with regional population dynamics.
Highlights
In hierarchically structured systems, natural selection can act at levels higher than the individual, such that individual fitness depends on the phenotypic expression of neighbours [1]
The quadratic and interaction terms of population and neighbour-population repertoire size were not significantly different from zero, nor did the size of the nearest patch have an effect (t = 0.61, P = 0.54). Both empirical studies and theoretical models have shown that group selection can contribute to evolutionary responses [2,58,59], neighbourhood effects and their populationlevel consequences are still poorly documented in the wild, especially in the context of metapopulations [16]
Evidence is almost nil for wild vertebrates, in spite of the fact that the wide application of capture-recapture models has permitted estimates of selection otherwise difficult to obtain in free living populations [60]
Summary
Natural selection can act at levels higher than the individual, such that individual fitness depends on the phenotypic expression of neighbours [1]. The selective value of a phenotype is a function of the trait expression of social partners, whereas with frequencydependent selection it depends on the relative phenotypic ranking of individuals within the group [2]. In the latter case, the number of individuals contributing to the generation in each group is independent of the mean group phenotype, while it is determined by group membership in group selection models [3]. Frequency dependence explains the maintenance of polymorphisms, clines or alternative strategies resulting from dynamic arms-races within groups [9]
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