From darkness to twilight: Morphological divergence between cave and surface-subterranean ecotone Niphargus species

Subterranean and surface habitats are in stark contrast in several environmental factors. Therefore, adaptation to the subterranean environment typically impedes the (re)colonisation of surface habitats. The genus Niphargus includes amphipod crustaceans that primarily occupy subterranean habitats. All its species show typical adaptations to the subterranean environment. However, some Niphargus species occur in surface-subterranean ecotones. To understand whether (i) habitat divergence is present between the cave and the ecotone species (ii) similar phenotypes emerge independently in every ecotone, we studied morphological divergence between four cave and four ecotone Niphargus species based on 13 functional morphological traits. To account for different selection acting on the sexes, we included males (N = 244) and females (N = 222). Nine out of 13 traits showed habitat- divergence. Traits related to feeding and crawling were shorter in ecotone species, while traits related to oxygenation were larger in ecotone species. Eleven out of 13 traits were sexually dimorphic. Traits related to oxygenation and crawling were larger in females, while the trait related to swimming was larger in males. We found that the extent of sexual dimorphism differs between the habitats in eight traits related to sensing, feeding, oxygenation and crawling. Additionally, we found that in certain traits related to sensing and oxygenation, habitat related differences are only present in case of one but not the other sex. We conclude that the detected differences between the cave and the ecotone species indicate divergent evolution, where similarities among the different species within a habitat type indicate convergent evolution. The high degree of sexual dimorphism paired with differences in sexual dimorphism between the habitats in certain traits suggest that sexual and fecundity selections have comparable effects to environmental selection. Thus, studies of habitat-dependent adaptations investigating one sex only, or not considering sexual dimorphism, can lead to erroneous conclusions. --

地下生境与地表生境在多项环境因子上存在显著差异。因此，适应地下生境通常会阻碍物种对地表生境的（再）定殖。泥钩虾属（Niphargus）包含主要栖息于地下生境的端足类甲壳动物，该属所有物种均展现出适应地下生境的典型特征。然而部分泥钩虾物种栖息于地表-地下生态交错带（ecotone）。为明确两点：一是洞穴物种与生态交错带物种之间是否存在生境分化；二是相似表型是否在各生态交错带中独立演化，我们基于13项功能形态学性状（functional morphological traits），对4种洞穴泥钩虾与4种生态交错带泥钩虾的形态分化展开了研究。为考量不同性别所受的选择压力差异，本研究纳入了244只雄性与222只雌性个体。13项性状中有9项呈现出生境相关的分化：生态交错带物种的取食与爬行相关性状长度更短，而其与氧合相关的性状则更长。13项性状中有11项存在雌雄二态性（sexually dimorphic）：雌性的氧合与爬行相关性状更大，而雄性的游泳相关性状则更发达。研究发现，在与感知、取食、氧合及爬行相关的8项性状中，雌雄二态性程度存在生境差异。此外，在部分与感知及氧合相关的性状中，生境相关的差异仅存在于单一性别中，而非两性均有体现。本研究结论为：洞穴物种与生态交错带物种间检出的差异指示了趋异演化，而同一生境类型下不同物种间的相似性则指示了趋同演化。高度的雌雄二态性，加上部分性状的雌雄二态性存在生境差异，表明性选择与繁殖力选择的效应与环境选择相当。因此，仅针对单一性别开展生境适应性研究，或未考虑雌雄二态性的相关研究，可能得出错误结论。