Triploid sterility drives somatic energy allocation in Pacific abalone (Haliotis discus hannai)

Triploid Pacific abalone ( Haliotis discus hannai ) are widely recognized for their remarkable growth superiority over diploids, yet the physiological mechanism bridging triploid sterility to this somatic growth advantage remains unclear. To address this knowledge gap, we reared diploid and triploid abalone cohorts under controlled dietary conditions (fed with either Gracilariopsis lemaneiformis or an artificial diet) for 24–30 months (From the ripening and spawning stages to the next gonadal growing stage). We systematically quantified key energetic traits, including foot muscle glycogen dynamics, tissue energy density (measured via bomb calorimetry), and tissue-specific energy allocation patterns, and employed Model II regression to model the energy transfer relationship between gonad and muscle tissues. Our results revealed that during gonadal maturation, triploids exhibited significantly higher foot muscle glycogen content compared to diploids: at 24 months post-fertilization (mpf, gonadal ripening and spawning stage), this difference was significant in the algae-fed group ( P < 0.05); by 30 mpf (gonadal growth stage), triploids in both dietary groups showed elevated glycogen levels ( P < 0.05). Notably, foot muscle glycogen content was inversely correlated with gonad bulk index (GBIn) in both ploidies, highlighting a link between gonad development and glycogen metabolism. Tissue energy analysis uncovered distinct energy partitioning strategies: triploids allocated 85.52 % of their total energy to foot muscle (versus 81.07 % in diploids) and only 7.25 % to gonads (versus 14.27 % in diploids). Model II regression further confirmed minimal energy transfer from muscle to gonad in triploids, evidenced by a positive correlation between gonad energy-FMSI residuals and foot muscle energy-FMSI residuals ( P < 0.05). In contrast, diploids showed a significant negative correlation between these residuals, indicating active muscle-to-gonad energy conversion to support reproduction. Collectively, these findings demonstrate that the growth superiority of triploid Pacific abalone is driven by sterility-induced somatic energy retention—a mechanism where energy otherwise allocated to gametogenesis in diploids is redirected to somatic tissues (e.g., foot muscle). This study not only advances our understanding of polyploidy-related physiological adaptations in shellfish but also provides a critical theoretical basis for optimizing triploid breeding strategies in commercially valuable abalone species. • Triploid sterility induces pronounced glycogen retention in foot muscle during gonadal maturation, contrasting with diploid depletion. • Energy allocation shifts decisively toward somatic tissues in triploids, reducing reproductive investment. • Model II regression confirms suppressed energy flux from muscle to gonad in triploids, mechanistically explaining growth superiority.

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Journal
Aquaculture Reports
Published
2025-11-27
DOI
https://doi.org/10.1016/j.aqrep.2025.103242
Primary Topic
Marine Bivalve and Aquaculture Studies
Type
article
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article

Triploid sterility drives somatic energy allocation in Pacific abalone (Haliotis discus hannai)

Jinwei Ke, Xuan Luo, Weiwei You, Jianpeng Zhang et al.
Aquaculture Reports
Marine Bivalve and Aquaculture Studies
article

Triploid sterility drives somatic energy allocation in Pacific abalone (Haliotis discus hannai)

Jinwei Ke, Xuan Luo, Weiwei You, Jianpeng Zhang, Caihuan Ke, Yi Wang
article en

Abstract

Triploid Pacific abalone ( Haliotis discus hannai ) are widely recognized for their remarkable growth superiority over diploids, yet the physiological mechanism bridging triploid sterility to this somatic growth advantage remains unclear. To address this knowledge gap, we reared diploid and triploid abalone cohorts under controlled dietary conditions (fed with either Gracilariopsis lemaneiformis or an artificial diet) for 24–30 months (From the ripening and spawning stages to the next gonadal growing stage). We systematically quantified key energetic traits, including foot muscle glycogen dynamics, tissue energy density (measured via bomb calorimetry), and tissue-specific energy allocation patterns, and employed Model II regression to model the energy transfer relationship between gonad and muscle tissues. Our results revealed that during gonadal maturation, triploids exhibited significantly higher foot muscle glycogen content compared to diploids: at 24 months post-fertilization (mpf, gonadal ripening and spawning stage), this difference was significant in the algae-fed group ( P < 0.05); by 30 mpf (gonadal growth stage), triploids in both dietary groups showed elevated glycogen levels ( P < 0.05). Notably, foot muscle glycogen content was inversely correlated with gonad bulk index (GBIn) in both ploidies, highlighting a link between gonad development and glycogen metabolism. Tissue energy analysis uncovered distinct energy partitioning strategies: triploids allocated 85.52 % of their total energy to foot muscle (versus 81.07 % in diploids) and only 7.25 % to gonads (versus 14.27 % in diploids). Model II regression further confirmed minimal energy transfer from muscle to gonad in triploids, evidenced by a positive correlation between gonad energy-FMSI residuals and foot muscle energy-FMSI residuals ( P < 0.05). In contrast, diploids showed a significant negative correlation between these residuals, indicating active muscle-to-gonad energy conversion to support reproduction. Collectively, these findings demonstrate that the growth superiority of triploid Pacific abalone is driven by sterility-induced somatic energy retention—a mechanism where energy otherwise allocated to gametogenesis in diploids is redirected to somatic tissues (e.g., foot muscle). This study not only advances our understanding of polyploidy-related physiological adaptations in shellfish but also provides a critical theoretical basis for optimizing triploid breeding strategies in commercially valuable abalone species. • Triploid sterility induces pronounced glycogen retention in foot muscle during gonadal maturation, contrasting with diploid depletion. • Energy allocation shifts decisively toward somatic tissues in triploids, reducing reproductive investment. • Model II regression confirms suppressed energy flux from muscle to gonad in triploids, mechanistically explaining growth superiority.

Aquaculture ReportsVol. 45
Guangxi University (CN), Xiamen University (CN), Guangxi Academy of Fishery Sciences (CN)
Openalex Percentile: Top 66%
Marine Bivalve and Aquaculture Studies
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