Data_Sheet_2_Reproductive Proteins Evolve Faster Than Non-reproductive Proteins Among Solanum Species.xlsx

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.

生殖蛋白进化速率升高是动物物种中的普遍观测结果，该现象被认为由专门作用于生殖性状的性选择（sexual selection）与性冲突（sexual conflict）所驱动。类似的进化模式是否广泛存在于其他生物类群中尚无定论。本研究以野生番茄物种（Solanum section Lycopersicon）为对象，探究该多样且快速进化的植物支系中生殖基因进化的驱动力量。通过比较生殖组织与非生殖组织中表达的基因座（locus，复数形式loci）的分子进化速率，本研究旨在验证以下假说：(a) 生殖特异性基因座的平均进化速率高于非生殖特异性基因座；(b) 雄性特异性基因座与雌性特异性基因座的进化速率存在差异；(c) 仅在配子体（gametophytic，单倍体haploid）组织中表达的基因，其进化模式与在孢子体（sporophytic，二倍体diploid）组织中表达的基因，或在两类组织中均表达的基因存在差异；(d) 交配系统变异（可作为性选择与性冲突预期强度的潜在替代指标）是否会影响蛋白进化模式。本研究观测到生殖蛋白的进化速率升高。但该模式在雌性特异性基因座中尤为显著，而非雄性特异性基因座，这一结论既适用于整体类群，也适用于推断受正向选择（positive selection）的单个基因座。生殖蛋白的进化速率升高可能得益于其更高的组织特异性，因为进化速率越快的基因，其表达范围往往越狭窄。与之相反，本研究未发现足够证据表明，经历单倍体选择的基因座（仅配子体表达基因座）的进化速率存在稳定差异，或是交配系统存在数量差异的支系间进化速率存在稳定差异。总体而言，尽管该多样植物类群的生殖蛋白进化速率普遍升高，但部分特定的进化模式比其他（主要为动物）系统中报道的更为复杂，其中在适应性进化的基因中，雌性特异性基因座发挥了更为突出的作用。