Data_Sheet_1_Reproductive Proteins Evolve Faster Than Non-reproductive Proteins Among Solanum Species.PDF

Elevated rates of evolution in reproductive proteins are commonly observed in animal species, and are thought to be driven by the action of sexual selection and sexual conflict acting specifically on reproductive traits. Whether similar patterns are broadly observed in other biological groups is equivocal. Here, we examine patterns of protein divergence among wild tomato species (Solanum section Lycopersicon), to understand forces shaping the evolution of reproductive genes in this diverse, rapidly evolving plant clade. By comparing rates of molecular evolution among loci expressed in reproductive and non-reproductive tissues, our aims were to test if: (a) reproductive-specific loci evolve more rapidly, on average, than non-reproductive loci; (b) ‘male’-specific loci evolve at different rates than ‘female’-specific loci; (c) genes expressed exclusively in gametophytic (haploid) tissue evolve differently from genes expressed in sporophytic (diploid) tissue or in both tissue types; and (d) mating system variation (a potential proxy for the expected strength of sexual selection and/or sexual conflict) affects patterns of protein evolution. We observed elevated evolutionary rates in reproductive proteins. However, this pattern was most evident for female- rather than male-specific loci, both broadly and for individual loci inferred to be positively selected. These elevated rates might be facilitated by greater tissue-specificity of reproductive proteins, as faster rates were also associated with more narrow expression domains. In contrast, we found little evidence that evolutionary rates are consistently different in loci experiencing haploid selection (gametophytic-exclusive loci), or in lineages with quantitatively different mating systems. Overall while reproductive protein evolution is generally elevated in this diverse plant group, some specific patterns of evolution are more complex than those reported in other (largely animal) systems, and include a more prominent role for female-specific loci among adaptively evolving genes.

在动物物种中，繁殖蛋白的进化速率普遍较高，并被认为是由性选择和性冲突对繁殖性状的特定作用所驱动。在其他生物群体中是否普遍观察到类似的模式尚无定论。本研究旨在探究野生番茄物种（Solanum section Lycopersicon）中蛋白质的分化模式，以理解塑造该多样且快速进化的植物类群繁殖基因进化的力量。通过比较繁殖和非繁殖组织中表达的位点的分子进化速率，我们的目标是检验以下假设：(a) 繁殖特异性位点的进化速度平均上比非繁殖位点更快；(b) '男性'特异性位点与'女性'特异性位点的进化速率不同；(c) 仅在配子体（单倍体）组织中表达的基因与在配子体（单倍体）组织或两种组织中表达的基因的进化不同；(d) 配子系统变异（可能作为预期性选择和/或性冲突强度的一种潜在代理）影响蛋白质进化的模式。我们观察到繁殖蛋白的进化速率有所提高。然而，这一模式在女性特异性位点而非男性特异性位点更为明显，无论是在广泛层面上还是在推断为正向选择的单个位点中。这些提高的速率可能得益于繁殖蛋白更强的组织特异性，因为较快的速率也与更窄的表达区域相关。相反，我们发现几乎没有证据表明经历单倍体选择的位点（配子体专属位点）或具有定量不同配子系统的谱系中的进化速率始终存在差异。总体而言，尽管在这个多样化的植物群体中繁殖蛋白的进化普遍较高，但某些进化模式比其他（主要动物）系统中的模式更为复杂，其中包括在适应性进化基因中女性特异性位点作用更为突出。