Sperm competition and sexually size dimorphic brains in birds

Abstract

Natural selection may favour sexually similar brain size owing to similar selection pressures in males and females, while sexual selection may lead to sexually dimorphic brains. For example, sperm competition involves clear-cut sex differences in behaviour, as males display, mate guard and copulate with females, while females choose among males, and solicit or reject copulations. These behaviours may require fundamentally different neural government in the two sexes leading to sex-dependent brain evolution. Using two phylogenetic approaches in a comparative study, we tested for roles of both natural and sexual-selection pressures on brain size evolution of birds. In accordance with the natural-selection theory, relative brain size of males coevolved with that of females, which may be the result of adaptation to similar environmental constraints such as feeding innovation. However, the mode of brain size evolution differed between the sexes, and factors associated with sperm competition as reflected by extra-pair paternity may give rise to sexually size dimorphic brains. Specifically, species in which females have larger brains than males were found to have a higher degree of extra-pair paternity independently of potentially confounding factors, whereas species in which males have relatively larger brains than females appeared to have lower rates of extra-pair paternity. Hence, the evolution of sperm competition may select for complex behaviours together with the associated neural substrates in the sex that has a higher potential to control extra-pair copulations at the observed levels. Brain function may thus be affected differently in males and females by sexual selection.

Figure 1

Relationship between relative brain size of female and male birds based on raw species data (F_1,160=813.684, p<0.001). The linear regression line is given (the corresponding equation: Y=0.962×X+0.014).

Figure 2

Interspecific relationship between frequencies of feeding innovation reported for European species and relative female brain size (filled circles) and male brain size (open triangles) based on raw species data. The solid line is for females, while the dashed line is for males, both representing linear regression lines. Corresponding statistics: relative female brain size: Kendall τ=0.278, p<0.001, n=74; relative male brain size: Kendall τ=0.311, p<0.001, n=74; relative brain size dimorphism: Kendall τ=−0.037, p=0.652, n=74.

Figure 3

Interspecific relationship between relative brain size dimorphism and extra-pair paternity in birds. (a) Raw species data with extra-pair paternity being square-root arcsine-transformed (F_1,37=6.641, p=0.014). (b) The relationship between relative brain size dimorphism and extra-pair paternity when the potentially confounding effects of sexual dichromatism and paternal care on extra-pair paternity were controlled in a multiple regression (dependent variable: brain size dimorphism, independent variables: extra-pair paternity sqrt-arcsine transformed, paternal care square-root arcsine-transformed, sexual dichromatism; overall F_3,25=3.031, p=0.051; extra-pair paternity, F_1,25=8.919, p=0.007; paternal care, F_1,25=0.784, p=0.385; sexual dichromatism, F_1,25=2.508, p=0.128). (c) The relationship between extra-pair paternity and sex-specific, relative brain sizes when covariation between male and female brain size was held constant in a multiple regression (dependent variable: extra-pair paternity, independent variables: relative brain size of females, relative brain size of males; overall F_3,37=3.733, p=0.034; relative brain size of females, F_1,37=4.438, p=0.042; relative brain size of males, F_1,37=7.000, p=0.012). The interaction term represents the association between brain size dimorphism and extra-pair paternity (see statistics above). We assessed the importance of extreme data points by calculating non-parametric correlations, thus based on ranked values, between relative brain size dimorphism and extra-pair paternity. This approach revealed similar results compared to the results based on parametric statistics ((a) Kendall τ=0.218, p=0.056, n=38; (b) Kendall τ=0.311, p=0.026, n=26; (c) females, Kendall τ=0.181, p=0.110, n=38; males, Kendall τ=−0.289, p=0.011, n=38). The linear regression lines are given. Filled circles and solid line are for females, while open triangles and dashed line are for males.