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<p>Global warming has accelerated range shifts in many marine species, exposing newly colonized populations to novel thermal environments. However, the molecular mechanisms that enable adaptations during distribution range expansion remain unclear. Here, we investigate the role of alternative splicing (AS) in thermal responses across four populations of the intertidal snail <i>Nerita yoldi</i> — two native (historical central Xiamen, XM; historical marginal Dongtou, DT) and two newly colonized (Lvsi, LS; Zhonganpeng, ZP) along a south-to-north latitudinal gradient reflecting the species’ recent northward range expansion along the Chinese coastline — using transcriptomic data from individuals exposed to control (25&#xa0;°C), moderate (37&#xa0;°C), and extreme (45&#xa0;°C) heat stress. The numbers of differential alternative splicing (DAS) events, DAS genes, and differentially expressed genes (DEGs), identified from within-population comparisons between heat-stressed (37&#xa0;°C or 45&#xa0;°C) and control conditions, increased with temperature in ZP, LS, and DT, but decreased in XM, revealing population-specific divergence in both transcriptional and post-transcriptional responses along the range expansion gradient. DEG and DAS gene sets showed near-complete non-redundancy, with transcription primarily adjusting bulk metabolic and immune processes and AS fine-tuned cell-cycle progression, cytoskeletal dynamics, and protein modification pathways, suggesting a complementary division of regulatory labour. GO enrichment analysis of DAS genes revealed largely population-specific functional profiles with limited overlap across populations, and the newly colonized populations exhibited consistent enrichment of immune response and proteostatic pathways at both temperatures. sQTL analysis identified only 9 DAS genes with fixed genetic divergence between populations (<i>F</i><sub>ST</sub> &gt; 0.2), indicating that the enhanced AS responses in marginal and expanded populations might be predominantly driven by environmentally induced plasticity rather than by fixed splicing-altering variants. Population-specific AS of splicing factors <i>srsf1b</i> and <i>mbnl1</i> further suggests that rewiring of the splicing machinery itself amplifies AS divergence across populations. Our findings suggest that AS represents a flexible and population-specific post-transcriptional regulatory layer underlying thermal adaptation during climate-driven range expansion, and highlight the necessity of integrating transcriptional and post-transcriptional analyses for a comprehensive understanding of molecular adaptation in expanding marine species.</p>

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Population-specific alternative splicing responses to heat stress in the range-expanding intertidal snail Nerita yoldii

  • 期刊论文

  • 发表日期：

    2026年6月22日

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  • Chao Zhai,
  • Jie Wang,
  • Yun-Wei Dong

摘要

Global warming has accelerated range shifts in many marine species, exposing newly colonized populations to novel thermal environments. However, the molecular mechanisms that enable adaptations during distribution range expansion remain unclear. Here, we investigate the role of alternative splicing (AS) in thermal responses across four populations of the intertidal snail Nerita yoldi — two native (historical central Xiamen, XM; historical marginal Dongtou, DT) and two newly colonized (Lvsi, LS; Zhonganpeng, ZP) along a south-to-north latitudinal gradient reflecting the species’ recent northward range expansion along the Chinese coastline — using transcriptomic data from individuals exposed to control (25 °C), moderate (37 °C), and extreme (45 °C) heat stress. The numbers of differential alternative splicing (DAS) events, DAS genes, and differentially expressed genes (DEGs), identified from within-population comparisons between heat-stressed (37 °C or 45 °C) and control conditions, increased with temperature in ZP, LS, and DT, but decreased in XM, revealing population-specific divergence in both transcriptional and post-transcriptional responses along the range expansion gradient. DEG and DAS gene sets showed near-complete non-redundancy, with transcription primarily adjusting bulk metabolic and immune processes and AS fine-tuned cell-cycle progression, cytoskeletal dynamics, and protein modification pathways, suggesting a complementary division of regulatory labour. GO enrichment analysis of DAS genes revealed largely population-specific functional profiles with limited overlap across populations, and the newly colonized populations exhibited consistent enrichment of immune response and proteostatic pathways at both temperatures. sQTL analysis identified only 9 DAS genes with fixed genetic divergence between populations (FST > 0.2), indicating that the enhanced AS responses in marginal and expanded populations might be predominantly driven by environmentally induced plasticity rather than by fixed splicing-altering variants. Population-specific AS of splicing factors srsf1b and mbnl1 further suggests that rewiring of the splicing machinery itself amplifies AS divergence across populations. Our findings suggest that AS represents a flexible and population-specific post-transcriptional regulatory layer underlying thermal adaptation during climate-driven range expansion, and highlight the necessity of integrating transcriptional and post-transcriptional analyses for a comprehensive understanding of molecular adaptation in expanding marine species.