Sankar Murugesan, Fraser Thomas W K, Nordvik Kari, Prabhu Philip Antony J, Remø Sofie, Hansen Tom J, Witten Paul Eckhard, Kryvi Harald, Fjelldal Per Gunnar
Reproduction and Developmental Biology Group, Institute of Marine Research, Matre Aquaculture Research Station, Matredal, Norway.
Department of Biological Sciences, University of Bergen, Bergen, Norway.
J Fish Biol. 2025 Mar;106(3):954-968. doi: 10.1111/jfb.16004. Epub 2024 Dec 4.
Atlantic salmon is an important aquaculture species that has fascinated naturalists for centuries, resulting in its biology being widely characterized. Certain details about the early development and the inheritance of meristic variation in the post-cranial axial skeleton are, however, largely unexplored. The present study gives a detailed description of the sequence of formation of the post-cranial axial skeleton based on whole-mount staining and used radiology to investigate the inheritance of meristic variation in isogenic hybrid all-male families of Atlantic salmon (~4 kg). Eight different families were created by crossing two homozygous double haploid XX females (dam A, B) with four different double haploid homozygous YY super males (sires a to d). In the caudal fin complex, the first bone to form is hypural 1 and its associated lepidotrichia followed by a bidirectional formation of new bones. In the dorsal and anal fins, development starts in the cranial part, and new bones form bidirectionally towards the head and tail fin. The neural and haemal arches start to form at segment 43, and further development is bidirectional. The first parapophysis form in the caudal part of the abdomen followed by a unidirectional completion cranially. The first ribs form at segment 3 and new ribs develop unidirectional caudally. Chordacentra formation starts at segment 24 followed by formation of chordacentrum number 58 (caudal-most vertebra). New chordacentrae form bidirectionally from segment 24 in parallel with the formation of chordacentrum number 57. The first epineuralia form at segment 1 followed by a unidirectional completion caudally until segment 30. The first supraneuralia to develop is number 10 closely followed by number 1, then new supraneurals form bidirectionally from number 10. Analysis of the inheritance on the post-cranial axial skeletal bones showed a strong maternal effect on total vertebrae centra and tail fin lepidotrichia counts. For these skeletal counts, dam A produced offspring with modes of 58 and 45 respectively, while dam B produced offspring with modes of 59 and 42. The higher number of total vertebrae centra produced by dam B was associated with additional abdominal and/or transitional vertebrae. The completion of formation in different post-cranial axial skeletal parts are either bi- or unidirectional, and the initiation of formation is site specific for each skeletal part with some inter-part similarities. Further, the present results may suggest that there has been a maternally driven selection for more abdominal vertebrae associated with a higher number of total vertebrae, and more tail fin lepidotrichia associated with a lower number of total vertebrae. These changing meristic counts may impact on important fitness-related traits, such as fecundity and swimming ability, making the present findings relevant for both ecological and aquaculture sciences.
大西洋鲑是一种重要的水产养殖品种,几个世纪以来一直吸引着博物学家,其生物学特性也得到了广泛的描述。然而,关于其早期发育以及颅后轴骨骼分节变异的遗传情况,某些细节在很大程度上仍未得到探索。本研究基于整体染色详细描述了颅后轴骨骼的形成顺序,并利用放射学研究了大西洋鲑(约4千克)同基因杂交全雄家系中分节变异的遗传情况。通过将两只纯合双单倍体XX雌性(母本A、B)与四只不同的双单倍体纯合YY超雄(父本a至d)杂交,创建了八个不同的家系。在尾鳍复合体中,首先形成的骨头是尾下骨1及其相关的鳞条,随后新骨头双向形成。在背鳍和臀鳍中,发育从头部开始,新骨头朝着头部和尾鳍双向形成。神经弓和血弓在第43节开始形成,进一步发育是双向的。第一对椎弓横突在腹部尾部形成,随后向头部单向完成。第一对肋骨在第3节形成,新肋骨向尾部单向发育。椎体中心的形成从第24节开始,随后形成第58个椎体中心(最尾端的椎骨)。新的椎体中心从第24节开始双向形成,与第57个椎体中心的形成同时进行。第一对神经上骨在第1节形成,随后向尾部单向完成,直到第30节。最早发育的上神经骨是第10个,紧接着是第1个,然后新的上神经骨从第10个开始双向形成。对颅后轴骨骼的遗传分析表明,在总椎体中心数和尾鳍鳞条数上存在强烈的母本效应。对于这些骨骼计数,母本A产生的后代模式分别为58和45,而母本B产生的后代模式为59和42。母本B产生的总椎体中心数较多与额外的腹部和/或过渡椎骨有关。不同颅后轴骨骼部分的形成完成方式要么是双向的,要么是单向的,并且每个骨骼部分的形成起始位置是特定的,部分之间存在一些相似性。此外,目前的结果可能表明,存在一种由母本驱动的选择,即选择更多与总椎体数较多相关的腹部椎骨,以及更多与总椎体数较少相关的尾鳍鳞条。这些不断变化的分节计数可能会影响重要的适应性相关性状,如繁殖力和游泳能力,使得本研究结果对生态科学和水产养殖科学都具有重要意义。