Digestive organ in the female reproductive tract borrows genes from multiple organ systems to adopt critical functions.
Digestive organ in the female reproductive tract borrows genes from multiple organ systems to adopt critical functions.
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DOI：
10.1093/molbev/msv048
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发表时间：
2015-06
影响因子：
10.7
通讯作者：
Clark NL
中科院分区：
文献类型：
--
作者：
Meslin C;Plakke MS;Deutsch AB;Small BS;Morehouse NI;Clark NL
持续的适应性挑战常常伴随着新的生理特征的进化而来。虽然有单个基因提供新的生理功能的具体例子，但对于复杂器官功能的起源缺乏研究。在鳞翅目昆虫的交配囊中就发现了一组这样的复杂功能，这是雌性生殖道中的一个器官，从雄性射精或精原细胞中消化营养物质。在这里，我们描述了法氏囊的生理和进化机制，通过这些机制，法氏囊具有消化和吸收功能。通过对法氏囊和其他八种组织的转录组的研究，我们发现了一套高表达和分泌的基因产物，为法氏囊提供了机械和酶消化男性精囊的胃样特征的组合。通过随后将这些法氏囊基因置于进化框架中，我们发现它们的绝大多数新的消化功能是通过借用在非生殖组织中继续表达的基因来实现的。然而，也出现了一些法氏囊特异的基因，其中一些代表了仅限于鳞翅目的独特基因家族，并可能提供新的法氏囊特异功能。这种杂乱的基因借用模式和相对罕见的组织特异性复制进化模式，与通过单基因共选来进化新颖性的研究形成了鲜明对比。我们的结果表明，复杂器官水平表型的进化可能经常被组织特异性的变化所启用(并随后受到限制)，这些变化允许现有基因在新的环境中表达，例如繁殖。在这些新角色中遇到的选择压力需要通过复制和亚/新功能化来解决的程度可能取决于对专门生殖功能的需求。因此，复杂的生理表型，如在法氏囊中发现的，为理解多效性和特化在适应性进化中的相对作用提供了重要的机会。
Persistent adaptive challenges are often met with the evolution of novel physiological traits. Although there are specific examples of single genes providing new physiological functions, studies on the origin of complex organ functions are lacking. One such derived set of complex functions is found in the Lepidopteran bursa copulatrix, an organ within the female reproductive tract that digests nutrients from the male ejaculate or spermatophore. Here, we characterized bursa physiology and the evolutionary mechanisms by which it was equipped with digestive and absorptive functionality. By studying the transcriptome of the bursa and eight other tissues, we revealed a suite of highly expressed and secreted gene products providing the bursa with a combination of stomach-like traits for mechanical and enzymatic digestion of the male spermatophore. By subsequently placing these bursa genes in an evolutionary framework, we found that the vast majority of their novel digestive functions were co-opted by borrowing genes that continue to be expressed in nonreproductive tissues. However, a number of bursa-specific genes have also arisen, some of which represent unique gene families restricted to Lepidoptera and may provide novel bursa-specific functions. This pattern of promiscuous gene borrowing and relatively infrequent evolution of tissue-specific duplicates stands in contrast to studies of the evolution of novelty via single gene co-option. Our results suggest that the evolution of complex organ-level phenotypes may often be enabled (and subsequently constrained) by changes in tissue specificity that allow expression of existing genes in novel contexts, such as reproduction. The extent to which the selective pressures encountered in these novel roles require resolution via duplication and sub/neofunctionalization is likely to be determined by the need for specialized reproductive functionality. Thus, complex physiological phenotypes such as that found in the bursa offer important opportunities for understanding the relative role of pleiotropy and specialization in adaptive evolution.