Thermal conditions during larval pelagic phase influence subsequent somatic growth of Senegalese sole by modulating gene expression and muscle growth dynamics

In the present study, Senegalese sole eggs incubated at 20 °C were reared at three different temperatures (15 °C, 18 °C or 21 °C) during the pelagic phase, and then transferred to a common temperature (20 °C) from benthic stage until 100 days post-hatch (dph). Somatic growth, fast muscle cellularity and expression of 15 growth-related genes were compared at the same developmental stage for each temperature (pre-metamorphic larvae, metamorphic larvae, post-metamorphic larvae) and at 83 dph and 100 dph early juveniles. During pre-metamorphosis and metamorphosis, larvae from 21 °C weighed significantly more than those reared at 18 °C or 15 °C (P < 0.001). Relative growth rate (RGR) of pelagic larvae and survival of newly-settled larvae were also higher at 21 °C (P < 0.05). Furthermore, an increase in muscle growth towards the highest temperatures was observed concomitantly with an increase in gene expression, namely myogenic regulatory factors (MRFs), myosins, igf-I and fgf6. After transfer to a common temperature (20 °C), the 15 °C group initiated a process of compensatory growth, inverting relative growth rate values that became the highest, particularly between 83 dph and 100 dph (P < 0.05). This increased growth effort in the 15 °C group was accompanied by an up-regulation of gene expression in fast muscle, particularly in the 83 dph juveniles. Mrf4 and myHC were up-regulated at 15 °C and positive correlations with growth were also found for myog or pax7 (P < 0.05). In contrast, mstn1 was down-regulated at 15 °C (P < 0.05), suggesting a boost in muscle growth. By 100 dph, the 15 °C group had already reached the same weight as the 18 °C and the same length as the 21 °C ones. At this age, the 18 °C juveniles had the largest mean muscle fibre diameter (P < 0.001), and thus fibre hypertrophy seems to be a major growth mechanism relatively to the other groups. Our work shows that temperature during pelagic phase greatly influences the growth trajectory of Senegalese sole juveniles.