Department of Biological Sciences, California State University, Los Angeles, CA 90032-8201, USA.
Department of Biological Sciences, California State University, Los Angeles, CA 90032-8201, USA.
Mol Phylogenet Evol. 2022 Sep;174:107523. doi: 10.1016/j.ympev.2022.107523. Epub 2022 May 16.
Host shifting in insect-plant systems was historically important to the development of ecological speciation theory, yet surprisingly few studies have examined whether host shifting drives diversification of marine herbivores. When small-bodied consumers feed and also mate on a preferred host, disruptive selection can split a population into host races despite gene flow. Support for host shifts is notably lacking for invertebrates associated with macroalgae, where the scale of dispersal by planktonic larvae often far exceeds the grain of host patchiness, and adults are typically less specialized than terrestrial herbivores. Here, we present a candidate example of ecological speciation in a clade of sea slugs that primarily consume green algae in the genus Caulerpa, including highly invasive species. Ancestral character state reconstructions supported 'sea grapes' (C. racemosa, C. lentillifera) as the ancestral host for a tropical radiation of 12 Elysia spp., with one shift onto alternative Caulerpa spp. in the Indo-Pacific. A Caribbean radiation of three species included symaptric host shifts to Rhipocephalus brevicaulis in the ancestor of E. pratensis Ortea & Espinosa, 1996, and to C. prolifera in E. hamanni Krug, Vendetti & Valdes 2016, plus a niche expansion to a range of Caulerpa spp. in E. subornata Verrill, 1901. All three species are broadly sympatric across the Caribbean but are host-partitioned at a fine grain, and distinct by morphology and at nuclear loci. However, non-recombining mtDNA revealed a history of gene flow between E. pratensis and E. subornata: COI haplotypes from E. subornata were 10.4% divergent from E. pratensis haplotypes from four sites, but closely related to all E. pratensis haplotypes sampled from six Bahamian islands, indicating historical introgression and localized "mitochondrial capture." Disruptive selective likely fueled divergence and adaptation to distinct host environments, indicating ecological speciation may be an under-appreciated driver of diversification for marine herbivores as well as epibionts and other resource specialists.
昆虫-植物系统中的宿主转移对生态物种形成理论的发展具有重要意义，但令人惊讶的是，很少有研究检查宿主转移是否推动了海洋草食动物的多样化。当小体型消费者在偏好的宿主上进食和交配时，尽管存在基因流，但离散选择可以将一个种群分裂成宿主种族。浮游幼虫的扩散规模通常远远超过宿主斑块的粒度，而且成虫通常不如陆生草食动物专业化，这使得与大型藻类相关的无脊椎动物的宿主转移支持明显不足。在这里，我们提出了一个候选的生态物种形成例子，即在一个主要以绿藻属 Caulerpa 为食的海蛞蝓类群中，包括高度入侵的物种。祖先特征状态重建支持“海葡萄”（C. racemosa，C. lentillifera）作为热带辐射的 12 种 Elysia spp.的祖先宿主，其中一种转移到印度洋-太平洋的替代 Caulerpa spp.。三种加勒比海辐射的物种包括在 E. pratensis Ortea & Espinosa, 1996 的祖先中向 Rhipocephalus brevicaulis 的共生宿主转移，以及在 E. hamanni Krug, Vendetti & Valdes 2016 中向 C. prolifera 的共生宿主转移，加上在一系列 Caulerpa spp.中的生态位扩张。在整个加勒比地区，这三个物种都广泛共存，但在精细的粒度上是宿主分区的，并且在形态和核基因座上是不同的。然而，非重组 mtDNA 揭示了 E. pratensis 和 E. subornata 之间的基因流历史：来自 E. subornata 的 COI 单倍型与来自四个地点的 E. pratensis 单倍型的差异为 10.4%，但与从六个巴哈马岛屿采样的所有 E. pratensis 单倍型密切相关，表明存在历史上的基因渗入和局部“线粒体捕获”。离散选择可能推动了分歧和对不同宿主环境的适应，这表明生态物种形成可能是海洋草食动物以及附生生物和其他资源专家多样化的一个被低估的驱动因素。
