Chow Lai Him, De Grave Sammy, Tsang Ling Ming
Simon F.S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Shatin, Hong Kong, China.
Oxford University Museum of Natural History, Parks Road, Oxford OX1 3PW, UK.
Mol Phylogenet Evol. 2021 Sep;162:107201. doi: 10.1016/j.ympev.2021.107201. Epub 2021 May 11.
Palaemonidae is the most speciose caridean shrimp family, with its huge biodiversity partially generated via symbiosis with various marine invertebrates. Previous studies have provided insights into the evolution of protective symbiosis in this family with evidence for frequent inter-phyla host switches, but the comprehensiveness of evolutionary pathways is hampered by the resolution of the previous phylogenetic trees as well as the taxon coverage. Furthermore, several critical issues related to the evolution of a symbiotic lifestyle, including the change in host spectrum and corresponding morphological adaptations, remain largely unresolved. We therefore performed a much extended phylogenetic comparative study on Palaemonidae, rooted in a comprehensive phylogeny reconstructed by a supermatrix-supertree approach based on a total of three mitochondrial and five nuclear markers. Ancestral state reconstruction of host associations revealed at least three independent evolutions into symbiosis, with potentially a drive to seek protection fuelling incipient symbiosis. Yet, most of the observed symbiotic species diversity was radiated from a single cnidarian associate. The evolution of mandibles and ambulatory dactyli suggests a general lack of correlation with host affiliation (except sponge endosymbionts), implying limited morphological adaptations following host switching, despite being putatively a major adaptive consequence of symbiosis. Our analyses of host spectrum, in terms of basic and taxonomic specificity, revealed no apparent phylogenetic signal but instead resolved a dynamic pattern attributable to frequent host switching. Uncoupling between host spectrum and the degree of morphological specialisation is the norm in palaemonids, suggesting that morphological characters are not fully in tune with host spectrum, in addition to host affiliation. This study demonstrates the complexity in the evolution of symbiosis, pointing to the presence of cryptic adaptations determining host spectrum and governing host switch diversification, and provides a clear direction for the evolutionary study of symbiosis in other marine symbiotic groups involving host switching.
长臂虾科是虾类中物种最为丰富的一个科，其巨大的生物多样性部分是通过与各种海洋无脊椎动物共生而产生的。先前的研究为该科保护性共生的进化提供了见解，有证据表明不同门类之间的宿主转换频繁，但先前系统发育树的分辨率以及分类群覆盖范围限制了进化途径的全面性。此外，与共生生活方式进化相关的几个关键问题，包括宿主谱的变化和相应的形态适应，在很大程度上仍未得到解决。因此，我们对长臂虾科进行了一项扩展得多的系统发育比较研究，该研究基于总共三个线粒体和五个核标记，通过超级矩阵 - 超级树方法重建了一个全面的系统发育。宿主关联的祖先状态重建显示，至少有三次独立的共生进化，可能是寻求保护的驱动力推动了初始共生。然而，观察到的大多数共生物种多样性是从单个刺胞动物共生体辐射而来的。颚和步足指节的进化表明，与宿主归属普遍缺乏相关性（海绵内共生体除外），这意味着尽管宿主转换被认为是共生的主要适应性后果，但宿主转换后形态适应有限。我们从基本特异性和分类特异性方面对宿主谱进行的分析没有发现明显的系统发育信号，反而解析出一种由频繁宿主转换导致的动态模式。在长臂虾科中，宿主谱与形态特化程度之间的解耦是常态，这表明除了宿主归属外，形态特征与宿主谱并不完全匹配。这项研究证明了共生进化的复杂性，指出存在决定宿主谱和控制宿主转换多样化的隐性适应，并为其他涉及宿主转换的海洋共生群体的共生进化研究提供了明确的方向。
