Sequence of formation and inheritance of meristic variation in the post-cranial axial skeleton of Atlantic salmon (Salmo salar)

Abstract

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.

Keywords: Atlantic salmon; inheritance; lepidotrich; meristic; pterygiophore; vertebra.

FIGURE 1

Schematic depiction of sequence of formation for the post‐cranial axial skeleton.

FIGURE 2

(a) Whole‐mount alizarine red staining showing formation of the first chordacentra (the first chordacentrum is indicated with a black asterisk). (b) Radiographic image of the anal fin in adult salmon. Pterygiophore and lepidotrich numbers are indicated.

FIGURE 3

Histograms of total vertebrae count split by dams and sires. Both dam and sire were in the final model, but there was no interaction.

FIGURE 4

Histograms of abdominal vertebrae count split by dams and sires. Both dam and sire were significant, but there was no interaction.

FIGURE 5

Histograms of transitional vertebrae count split by dams and sires. Both dam and sire were significant, but there was no interaction.

FIGURE 6

Histograms of caudal vertebrae count split by dams and sires. Only the sire was significant.

FIGURE 7

Histograms of ural vertebrae count split by dams and sires. Only the dam was significant.

FIGURE 8

Histograms of anal fin lepidotrichia split by dam. Only the dam was significant.

FIGURE 9

Histograms of anal fin ray (lepidotrich) counts split by dam. Only the dam was significant.

FIGURE 10

Histograms of tail fin ray (lepidotrich) counts split by dam and sire. Both dam and sire were significant, but there was no interaction.

FIGURE 11

Correlation matrix of the general population (all families). The lower triangle contains the r values (from a Spearman's rank correlation) while the upper triangle is a visual representation of the strength of the relationships indicated by the size (stronger relationships are more elliptical) and color (blue for positive, red for negative) of the ellipses. The asterisks in the upper panel indicate tests which were significant; *p < 0.05, **p < 0.01, ***p < 0.001. AL, anal fin lepidotrichia; AP, anal fin pterygiophores; DL, dorsal fin lepidotrichia; DP, dorsal fin pterygiophores; TL, tail fin lepidotrichia.