Development of the cranial lateral line system of Brook Trout, Salvelinus fontinalis (Teleostei: Salmonidae): Evolutionary and ecological implications

IF 1.5 4区 医学 Q2 ANATOMY & MORPHOLOGY
Aubree E. Jones, Pedro P. Rizzato, Jacqueline F. Webb
{"title":"Development of the cranial lateral line system of Brook Trout, Salvelinus fontinalis (Teleostei: Salmonidae): Evolutionary and ecological implications","authors":"Aubree E. Jones,&nbsp;Pedro P. Rizzato,&nbsp;Jacqueline F. Webb","doi":"10.1002/jmor.21754","DOIUrl":null,"url":null,"abstract":"<p>The mechanosensory lateral line (LL) system of salmonid fishes has been the focus of comparative morphological studies and behavioral and physiological analyses of flow sensing capabilities, but its morphology and development have not been studied in detail in any one species. Here, we describe the post-embryonic development of the cranial LL system in Brook Trout, <i>Salvelinus fontinalis</i>, using vital fluorescent staining (4-Di-2-ASP), scanning electron microscopy, µCT, and clearing and staining to visualize neuromasts and the process of cranial LL canal morphogenesis. We examined the relationship between the timing of LL development, the prolonged life history of salmonids, and potential ecological implications. The LL system is composed of seven canals containing canal neuromasts (CNs) and four lines of superficial neuromasts (SNs) on the skin. CNs and SNs increase in number and size during the alevin (larval) stage. CN number stabilizes as canal morphogenesis commences, but SN number increases well into the parr (juvenile) stage. CNs become larger and more elongated than SNs, but the relative area occupied by sensory hair cells decreases during ontogeny in both types of neuromasts. Neuromast-centered canal morphogenesis starts in alevins (yolk sac larvae), as they swim up into the water column from their gravel nests (~4 months post-fertilization), after which yolk sac absorption is completed and exogenous feeding begins. Canal morphogenesis proceeds asynchronously within and among canal series and is not complete until ~8 months post-fertilization (the parr stage). Three characters in the LL system and associated dermal bones were used to identify their homologs in other actinopterygians and to consider the evolution of LL canal reduction, thus demonstrating the value of salmonids for the study of LL evolution. The prolonged life history of Brook Trout and the onset of canal morphogenesis at swim-up are predicted to have implications for neuromast function at these critical behavioral and ecological transitions.</p>","PeriodicalId":16528,"journal":{"name":"Journal of Morphology","volume":"285 8","pages":""},"PeriodicalIF":1.5000,"publicationDate":"2024-08-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Morphology","FirstCategoryId":"3","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1002/jmor.21754","RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"ANATOMY & MORPHOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

The mechanosensory lateral line (LL) system of salmonid fishes has been the focus of comparative morphological studies and behavioral and physiological analyses of flow sensing capabilities, but its morphology and development have not been studied in detail in any one species. Here, we describe the post-embryonic development of the cranial LL system in Brook Trout, Salvelinus fontinalis, using vital fluorescent staining (4-Di-2-ASP), scanning electron microscopy, µCT, and clearing and staining to visualize neuromasts and the process of cranial LL canal morphogenesis. We examined the relationship between the timing of LL development, the prolonged life history of salmonids, and potential ecological implications. The LL system is composed of seven canals containing canal neuromasts (CNs) and four lines of superficial neuromasts (SNs) on the skin. CNs and SNs increase in number and size during the alevin (larval) stage. CN number stabilizes as canal morphogenesis commences, but SN number increases well into the parr (juvenile) stage. CNs become larger and more elongated than SNs, but the relative area occupied by sensory hair cells decreases during ontogeny in both types of neuromasts. Neuromast-centered canal morphogenesis starts in alevins (yolk sac larvae), as they swim up into the water column from their gravel nests (~4 months post-fertilization), after which yolk sac absorption is completed and exogenous feeding begins. Canal morphogenesis proceeds asynchronously within and among canal series and is not complete until ~8 months post-fertilization (the parr stage). Three characters in the LL system and associated dermal bones were used to identify their homologs in other actinopterygians and to consider the evolution of LL canal reduction, thus demonstrating the value of salmonids for the study of LL evolution. The prolonged life history of Brook Trout and the onset of canal morphogenesis at swim-up are predicted to have implications for neuromast function at these critical behavioral and ecological transitions.

Abstract Image

布鲁克斯鳟鱼(Salvelinus fontinalis,远洋鱼类:鲑科)颅侧线系统的发育:进化和生态学意义
鲑科鱼类的机械感觉侧线(LL)系统一直是流感应能力的比较形态学研究、行为学和生理学分析的重点,但其形态和发育尚未在任何一个物种中得到详细研究。在这里,我们描述了溪鳟鱼(Salvelinus fontinalis)颅骨LL系统胚胎后的发育过程,利用重要的荧光染色(4-Di-2-ASP)、扫描电子显微镜、µCT和清除染色来观察神经细胞和颅骨LL管的形态发生过程。我们研究了 LL 发育的时间、鲑鱼漫长的生活史和潜在的生态影响之间的关系。鳞状神经管系统由包含鳞状神经管(CN)和皮肤上的四列表层神经管(SN)的七个神经管组成。在幼虫阶段,CN 和 SN 的数量和大小都会增加。随着管状形态发生的开始,CN 的数量趋于稳定,但 SN 的数量一直增加到 parr(幼体)阶段。CN比SN更大、更长,但在两种神经母细胞的发育过程中,感觉毛细胞所占的相对面积都在减少。以神经母细胞为中心的管状体形态发生始于卵黄囊幼体(levins),当它们从砾石巢游入水体时(受精后约 4 个月),卵黄囊吸收完成,外源摄食开始。管系内和管系间的形态发生不同步,直到受精后约 8 个月(parr 阶段)才完成。我们利用 LL 系统和相关真皮骨中的三个特征来确定它们在其他动口纲动物中的同源物,并考虑 LL 管缩小的进化,从而证明了鲑科鱼类在研究 LL 进化方面的价值。布鲁克鳟的生活史较长,在游泳时开始管状形态发生,预计在这些关键的行为和生态过渡时期对神经嵴的功能有影响。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Journal of Morphology
Journal of Morphology 医学-解剖学与形态学
CiteScore
2.80
自引率
6.70%
发文量
119
审稿时长
1 months
期刊介绍: The Journal of Morphology welcomes articles of original research in cytology, protozoology, embryology, and general morphology. Articles generally should not exceed 35 printed pages. Preliminary notices or articles of a purely descriptive morphological or taxonomic nature are not included. No paper which has already been published will be accepted, nor will simultaneous publications elsewhere be allowed. The Journal of Morphology publishes research in functional, comparative, evolutionary and developmental morphology from vertebrates and invertebrates. Human and veterinary anatomy or paleontology are considered when an explicit connection to neontological animal morphology is presented, and the paper contains relevant information for the community of animal morphologists. Based on our long tradition, we continue to seek publishing the best papers in animal morphology.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信