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Background <p>Niemann-Pick type C2 (NPC2) proteins have been proposed as soluble carriers for semiochemicals in arthropods, serving as putative functional substitutes for the canonical odorant-binding proteins (OBPs) largely absent in arachnids. However, the evolutionary mechanisms driving NPC2 diversification in spiders—particularly in ambush predators relying heavily on chemical cues—remain unclear.</p> Results <p>We identified a minimum expressed repertoire of 13 high-confidence <i>NPC2</i> genes in the crab spider <i>Ebrechtella tricuspidata</i> via comprehensive transcriptomic profiling. Comparative phylogenomics across 21 arthropod species revealed that while the generalist herbivore mite <i>Tetranychus urticae</i> underwent a significant repertoire expansion (+ 9 genes, <i>P</i> &lt; 0.001), the <i>E. tricuspidata</i> lineage exhibited a modest numerical gain (+ 3 genes). Despite this, transcriptomic data revealed a striking functional dichotomy within the spider repertoire. The basal singleton <i>EtriNPC2-2</i> was highly enriched in the abdomen, suggesting a conserved role in visceral lipid transport. In contrast, the derived <i>Etri-B</i> subclade (<i>EtriNPC2-1</i>,<i> -3</i>) and the singleton <i>EtriNPC2-4</i> were predominantly expressed in chemosensory appendages (palps and legs). This spatial expression shift coincided with strong signatures of episodic positive selection acting on the <i>Etri-B</i> lineage. Structural modeling identified a key adaptive substitution (L33→Q31) at the pocket entrance of EtriNPC2-3, serving as a prime candidate for future functional validation regarding ligand access in the sensillar lymph.</p> Conclusions <p>Our findings suggest a clear pattern of neofunctionalization, where gene duplication enabled spider <i>NPC2s</i> to diverge from an ancestral visceral function toward a specialized sensory role. This linkage between spatial expression shifts and adaptive sequence evolution provides essential molecular evidence for how ambush spiders evolved a complex chemosensory system in the absence of insect-type OBPs.</p>

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Lineage-specific expansion and positive selection of NPC2 genes in the crab spider Ebrechtella tricuspidata and other arachnids

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2026年3月28日

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  • Tianlei Liu,
  • Chunlei Cong,
  • Jianxin Chen,
  • Daochao Jin

摘要

Background

Niemann-Pick type C2 (NPC2) proteins have been proposed as soluble carriers for semiochemicals in arthropods, serving as putative functional substitutes for the canonical odorant-binding proteins (OBPs) largely absent in arachnids. However, the evolutionary mechanisms driving NPC2 diversification in spiders—particularly in ambush predators relying heavily on chemical cues—remain unclear.

Results

We identified a minimum expressed repertoire of 13 high-confidence NPC2 genes in the crab spider Ebrechtella tricuspidata via comprehensive transcriptomic profiling. Comparative phylogenomics across 21 arthropod species revealed that while the generalist herbivore mite Tetranychus urticae underwent a significant repertoire expansion (+ 9 genes, P < 0.001), the E. tricuspidata lineage exhibited a modest numerical gain (+ 3 genes). Despite this, transcriptomic data revealed a striking functional dichotomy within the spider repertoire. The basal singleton EtriNPC2-2 was highly enriched in the abdomen, suggesting a conserved role in visceral lipid transport. In contrast, the derived Etri-B subclade (EtriNPC2-1, -3) and the singleton EtriNPC2-4 were predominantly expressed in chemosensory appendages (palps and legs). This spatial expression shift coincided with strong signatures of episodic positive selection acting on the Etri-B lineage. Structural modeling identified a key adaptive substitution (L33→Q31) at the pocket entrance of EtriNPC2-3, serving as a prime candidate for future functional validation regarding ligand access in the sensillar lymph.

Conclusions

Our findings suggest a clear pattern of neofunctionalization, where gene duplication enabled spider NPC2s to diverge from an ancestral visceral function toward a specialized sensory role. This linkage between spatial expression shifts and adaptive sequence evolution provides essential molecular evidence for how ambush spiders evolved a complex chemosensory system in the absence of insect-type OBPs.