Artieri Carlo G, Haerty Wilfried, Singh Rama S
Department of Biology, McMaster University, Hamilton, Ontario, Canada.
BMC Biol. 2009 Jul 21;7:42. doi: 10.1186/1741-7007-7-42.
Karl Ernst Von Baer noted that species tend to show greater morphological divergence in later stages of development when compared to earlier stages. Darwin originally interpreted these observations via a selectionist framework, suggesting that divergence should be greatest during ontogenic stages in which organisms experienced varying 'conditions of existence' and opportunity for differential selection. Modern hypotheses have focused on the notion that genes and structures involved in early development will be under stronger purifying selection due to the deleterious pleiotropic effects of mutations propagating over the course of ontogeny, also known as the developmental constraint hypothesis.
Using developmental stage-specific expressed sequence tag (EST) libraries, we tested the 2 hypotheses by comparing the rates of evolution of 7,180 genes obtained from 6 species of the Drosophila melanogaster group with respect to ontogeny, and sex and reproduction-related functions in gonadal tissues. Supporting morphological observations, we found evidence of a pattern of increasing mean evolutionary rate in genes that are expressed in subsequent stages of development. Furthermore, supporting expectations that early expressed genes are constrained in divergence, we found that embryo stage genes are involved in a higher mean number of interactions as compared to later stages. We noted that the accelerated divergence of genes in the adult stage is explained by those expressed specifically in the male gonads, whose divergence is driven by positive selection. In addition, accelerated gonadal gene divergence occurs only in the adult stage, suggesting that the effects of selection are observed primarily at the stages during which they are expected occur. Finally, we also found a significant correlation between temporal specificity of gene expression and evolutionary rate, supporting expectations that genes with ubiquitous expression are under stronger constraint.
Taken together, these results support both the developmental constraint hypothesis limiting the divergence of early expressed developmentally important genes, leading to a gradient of divergence rates over ontogeny (embryonic < larval/pupal < adult), as well as Darwin's 'selection opportunity' hypothesis leading to increased divergence in adults, particularly in the case of reproductive tissues. We suggest that a constraint early/opportunity late model best explains divergence over ontogeny.
卡尔·恩斯特·冯·贝尔指出，与早期阶段相比，物种在发育后期往往表现出更大的形态差异。达尔文最初通过选择主义框架来解释这些观察结果，认为在个体发育阶段，当生物体经历不同的“生存条件”和差异选择机会时，差异应该最大。现代假说则聚焦于这样一种观点，即由于突变在个体发育过程中传播产生的有害多效性影响，参与早期发育的基因和结构将受到更强的纯化选择，这也被称为发育限制假说。
利用发育阶段特异性表达序列标签（EST）文库，我们通过比较从黑腹果蝇组的6个物种中获得的7180个基因在个体发育、性腺组织中的性别和生殖相关功能方面的进化速率，对这两个假说进行了检验。支持形态学观察结果的是，我们发现了在发育后期表达的基因中平均进化速率增加的模式的证据。此外，支持早期表达基因在差异上受到限制的预期，我们发现与后期阶段相比，胚胎期基因参与的相互作用平均数量更多。我们注意到，成年期基因的加速差异是由那些在雄性性腺中特异性表达的基因所解释的，其差异是由正选择驱动的。此外，性腺基因的加速差异仅发生在成年期，这表明选择的影响主要在预期发生的阶段被观察到。最后，我们还发现基因表达的时间特异性与进化速率之间存在显著相关性，支持了普遍表达的基因受到更强限制的预期。
综上所述，这些结果既支持发育限制假说，即限制早期表达的发育重要基因的差异，导致个体发育过程中差异速率的梯度（胚胎期<幼虫/蛹期<成年期），也支持达尔文的“选择机会”假说，即导致成年期差异增加，特别是在生殖组织的情况下。我们认为，早期限制/后期机会模型最能解释个体发育过程中的差异。
