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Flexible conservatism in the skull modularity of convergently evolved myrmecophagous placental mammals
BMC Ecology and Evolution ( IF 2.3 ) Pub Date : 2022-06-30 , DOI: 10.1186/s12862-022-02030-9
Sérgio Ferreira-Cardoso 1 , Julien Claude 1 , Anjali Goswami 2 , Frédéric Delsuc 1 , Lionel Hautier 1, 2
Affiliation  

The skull of placental mammals constitutes one of the best studied systems for phenotypic modularity. Several studies have found strong evidence for the conserved presence of two- and six-module architectures, while the strength of trait correlations (integration) has been associated with major developmental processes such as somatic growth, muscle-bone interactions, and tooth eruption. Among placentals, ant- and termite-eating (myrmecophagy) represents an exemplar case of dietary convergence, accompanied by the selection of several cranial morphofunctional traits such as rostrum elongation, tooth loss, and mastication loss. Despite such drastic functional modifications, the covariance patterns of the skull of convergently evolved myrmecophagous placentals are yet to be studied in order to assess the potential consequences of this dietary shift on cranial modularity. Here, we performed a landmark-based morphometric analysis of cranial covariance patterns in 13 species of myrmecophagous placentals. Our analyses reveal that most myrmecophagous species present skulls divided into six to seven modules (depending on the confirmatory method used), with architectures similar to those of non-myrmecophagous placentals (therian six modules). Within-module integration is also similar to what was previously described for other placentals, suggesting that most covariance-generating processes are conserved across the clade. Nevertheless, we show that extreme rostrum elongation and tooth loss in myrmecophagid anteaters have resulted in a shift in intermodule correlations in the proximal region of the rostrum. Namely, the naso-frontal and maxillo-palatine regions are strongly correlated with the oro-nasal module, suggesting an integrated rostrum conserved from pre-natal developmental processes. In contrast, the similarly toothless pangolins show a weaker correlation between the anterior rostral modules, resembling the pattern of toothed placentals. These results reveal that despite some integration shifts related to extreme functional and morphological features of myrmecophagous skulls, cranial modular architectures have conserved the typical mammalian scheme.

中文翻译:

趋同进化的食虫胎盘哺乳动物颅骨模块化的灵活保守性

胎盘哺乳动物的头骨是表型模块化研究最好的系统之一。几项研究发现了两个和六个模块结构的保守存在的有力证据,而性状相关性(整合)的强度与主要发育过程有关,例如体细胞生长、肌肉-骨骼相互作用和牙齿萌出。在胎盘中,以蚂蚁和白蚁为食(myrmecophagy)代表了饮食趋同的典型案例,伴随着对几种颅骨形态功能特征的选择,例如喙伸长、牙齿脱落和咀嚼缺失。尽管进行了如此剧烈的功能修改,为了评估这种饮食转变对颅骨模块性的潜在影响,尚未研究趋同进化的食虫胎盘颅骨的协方差模式。在这里,我们对 13 种 myrmecophagous 胎盘中的颅协方差模式进行了基于地标的形态计量分析。我们的分析表明,大多数食虫动物的头骨分为 6 到 7 个模块(取决于使用的确认方法),其结构类似于非食虫胎盘(有 6 个模块)。模块内整合也类似于先前对其他胎盘的描述,这表明大多数协方差产生过程在进化枝中是保守的。尽管如此,我们表明,食蚁兽食蚁兽的极端伸长和牙齿脱落导致了喙近端区域模块间相关性的变化。即,鼻额和上颌腭区域与口鼻模块密切相关,表明从产前发育过程中保存的综合讲台。相比之下,类似无牙的穿山甲显示前喙模块之间的相关性较弱,类似于带齿胎盘的模式。这些结果表明,尽管与食虫头骨的极端功能和形态特征相关的一些整合变化,颅骨模块化结构保留了典型的哺乳动物方案。鼻额和上颌腭区域与口鼻模块密切相关,表明从产前发育过程中保存的综合讲台。相比之下,类似无牙的穿山甲显示前喙模块之间的相关性较弱,类似于带齿胎盘的模式。这些结果表明,尽管与食虫头骨的极端功能和形态特征相关的一些整合变化,颅骨模块化结构保留了典型的哺乳动物方案。鼻额和上颌腭区域与口鼻模块密切相关,表明从产前发育过程中保存的综合讲台。相比之下,类似无牙的穿山甲显示前喙模块之间的相关性较弱,类似于带齿胎盘的模式。这些结果表明,尽管与食虫头骨的极端功能和形态特征相关的一些整合变化,颅骨模块化结构保留了典型的哺乳动物方案。
更新日期:2022-07-01
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