Hard to get, easy to lose: Evolution of mantle photoreceptor organs in bivalves (Bivalvia, Pteriomorphia)

Morphologically diverse eyes have evolved numerous times, yet little is known about how eye gain and loss is related to photic environment. The pteriomorphian bivalves (e.g., oysters, scallops, and ark clams), with a remarkable range of photoreceptor organs and ecologies, are a suitable system to investigate the association between eye evolution and ecological shifts. The present phylogenetic framework was based on amino acid sequences from transcriptome datasets and nucleotide sequences of five additional genes. In total, 197 species comprising 22 families from all five pteriomorphian orders were examined, representing the greatest taxonomic sampling to date. Morphological data were acquired for 162 species and lifestyles were compiled from the literature for all 197 species. Photoreceptor organs occur in 11 families and have arisen exclusively in epifaunal lineages, i.e., living above the substrate, at least five times independently. Models for trait evolution consistently recovered higher rates of loss over gain. Transitions to crevice-dwelling habit appear associated with convergent gains of eyespots in epifaunal lineages. Once photoreceptor organs have arisen, multiple losses occurred in lineages that shift to burrowing lifestyles and deep-sea habitats. The observed patterns suggest that eye evolution in pteriomorphians might have evolved in association with light-guided behaviors, such as phototaxis, body posture, and alarm responses.

Methods
Dataset for 197 pteriomorphian species and eight other bivalve species, including amino acid sequences (from 277 orthologs in Matrix 2, see Lemer et al. 2016) and five additional nucleotide sequences (16S rRNA, COI,18S rRNA, 28S rRNA, and Histone H3) available in GenBank. All molecular data with respective accession numbers are listed in supporting information (Table S1). Alignments were performed in MAFFT v7.311 under the L-INS-i method (Katoh and Standley 2013). The phylogenetic tree file (nexus format) was obtained in a partitioned analysis performed in IQ-TREE v1.6.12 (Nguyen et al. 2014) under maximum likelihood and the following models of sequence evolution: GTR+I+G (for nucleotide sequences) and LG+F+I+G (for amino acid sequences from the transcriptome dataset).

形态多样的眼睛已独立演化多次，但学界对眼睛的起源与丢失如何与光照环境（photic environment）相关联仍所知甚少。翼形类双壳类（pteriomorphian bivalves，如牡蛎、扇贝及蚶类）拥有范围极广的感光器官与生态类群，是探究眼睛演化与生态转变之间关联的理想研究体系。本研究的系统发育框架基于转录组数据集得到的氨基酸序列，以及另外5个基因的核苷酸序列。本次研究共涵盖5个翼形目下22个科的197个物种，为迄今规模最大的类群采样。我们为162个物种获取了形态学数据，并从文献中整理了全部197个物种的生活方式信息。感光器官分布于11个科中，且仅在底栖附着（epifaunal，即栖息于基质上方）的支系中出现，至少独立起源了5次。性状演化模型一致显示，眼睛的丢失速率显著高于起源速率。向缝隙栖息习性的转变，似乎与底栖附着支系中眼斑的趋同获得相关。一旦感光器官演化形成，在转向穴居生活方式与深海生境的支系中便发生了多次丢失事件。本研究观察到的模式表明，翼形类双壳类的眼睛演化可能与趋光行为相关联，例如趋光性、躯体姿态调节及警报反应。

方法
本数据集涵盖197个翼形类物种及另外8个双壳类物种，包含转录组数据集得到的氨基酸序列（来自Matrix 2中的277个直系同源基因（orthologs），详见Lemer等2016年研究），以及另外5个核苷酸序列：16S rRNA、COI、18S rRNA、28S rRNA及组蛋白H3，上述序列均可在GenBank中获取。所有带对应登录号（accession numbers）的分子数据均列于补充材料（表S1）。序列比对使用MAFFT v7.311软件的L-INS-i方法完成（Katoh与Standley，2013）。系统发育树文件（nexus格式）通过IQ-TREE v1.6.12软件进行分区最大似然分析得到，采用的序列演化模型分别为：核苷酸序列使用GTR+I+G模型，转录组数据集的氨基酸序列使用LG+F+I+G模型（Nguyen等2014年研究）。