Sex-specific natural selection on SNPs in Silene latifolia

Abstract

Selection that acts in a sex-specific manner causes the evolution of sexual dimorphism. Sex-specific phenotypic selection has been demonstrated in many taxa and can be in the same direction in the two sexes (differing only in magnitude), limited to one sex, or in opposing directions (antagonistic). Attempts to detect the signal of sex-specific selection from genomic data have confronted numerous difficulties. These challenges highlight the utility of "direct approaches," in which fitness is predicted from individual genotype within each sex. Here, we directly measured selection on Single Nucleotide Polymorphisms (SNPs) in a natural population of the sexually dimorphic, dioecious plant, Silene latifolia. We measured flowering phenotypes, estimated fitness over one reproductive season, as well as survival to the next year, and genotyped all adults and a subset of their offspring for SNPs across the genome. We found that while phenotypic selection was congruent (fitness covaried similarly with flowering traits in both sexes), SNPs showed clear evidence for sex-specific selection. SNP-level selection was particularly strong in males and may involve an important gametic component (e.g., pollen competition). While the most significant SNPs under selection in males differed from those under selection in females, paternity selection showed a highly polygenic tradeoff with female survival. Alleles that increased male mating success tended to reduce female survival, indicating sexual antagonism at the genomic level. Perhaps most importantly, this experiment demonstrates that selection within natural populations can be strong enough to measure sex-specific fitness effects of individual loci. Males and females typically differ phenotypically, a phenomenon known as sexual dimorphism. These differences arise when selection on males differs from selection on females, either in magnitude or direction. Estimated relationships between traits and fitness indicate that sex-specific selection is widespread, occurring in both plants and animals, and explains why so many species exhibit sexual dimorphism. Finding the specific loci experiencing sex-specific selection is a challenging prospect but one worth undertaking given the extensive evolutionary consequences. Flowering plants with separate sexes are ideal organisms for such studies, given that the fitness of females can be estimated by counting the number of seeds they produce. Determination of fitness for males has been made easier as thousands of genetic markers can now be used to assign paternity to seeds. We undertook just such a study in S. latifolia, a short-lived, herbaceous plant. We identified loci under sex-specific selection in this species and found more loci affecting fitness in males than females. Importantly, loci with major effects on male fitness were distinct from the loci with major effects on females. We detected sexual antagonism only when considering the aggregate effect of many loci. Hence, even though males and females share the same genome, this does not necessarily impose a constraint on their independent evolution.

Keywords: dioecious; fitness; paternity; selection component analysis; sexual dimorphism; sex‐specific selection.

Figure 1

Top panel: Silene latifolia flowers from our study site: female (left) and male (right). Flowers open at dusk and are pollinated by night‐flying moths (Jürgens et al. 1996). Flowers on females have wider calyces, weigh more, and are fewer in number than those on males (Delph 2007). Bottom panel: view of the clearing in early spring 2018, showing the pipe that was laid in 2015.

Figure 2

The relationship between our two fitness measures (paternity [number of offspring sired by males] and the number of seeds produced [females]), two flowering traits, and survival. Top panel: natural log of the number of days each plant flowered in 2018. Middle panel: natural log of the total number of flowers produced in 2018. The linear regression slopes (b) and Spearman correlations (ρ) are reported for each contrast. Bottom panel: the state of each plant in 2019 (box plots show the medium value, the first and third quartile, the whiskers, and outliers). The point for one female plant is not shown (although the data were included for analyses); over a 22‐day period (Ln value = 3.09), this plant, which was alive in 2019, produced 8539 seeds from 160 flowers (Ln value = 5.08).

Figure 3

The relationship between Δq from paternity selection and the other four components of selection: (A) male selection, (B) Female fecundity selection, (C) male survival, and (D) female survival. Red points denote the 53 SNPs that were genome‐wide significant (FDR < 0.1) for paternity selection (jiggered to show all 53 SNPs). In (B), blue points are the 13 SNPs significant for seed production in females. The lines were calculated by least squares but association tests on all SNPs were based on permutation using the Spearman correlation as a test statistic. The solid lines (A and D) denote statistically significant associations.