Is permanent parasitism reversible? – Critical evidence from early evolution of house dust mites

Long-term specialization may limit the ability of a species to respond to new environmental conditions and lead to a higher likelihood of extinction. For permanent parasites and other symbionts, the most intriguing question is whether these organisms can return to a free-living lifestyle and, thus, escape an evolutionary ‘dead end’. This question is directly related to Dollo's law, which stipulates that a complex trait (such as being free-living vs. parasitic) cannot re-evolve again in the same form. Here we present conclusive evidence that house dust mites, a group of medically important free-living organisms, evolved from permanent parasites of warm-blooded vertebrates. A robust, multigene topology (315 taxa, 8,942 nt), ancestral character state reconstruction, and a test for irreversible evolution (Dollo's law) demonstrate that house dust mites have abandoned a parasitic lifestyle, secondarily becoming free-living, and then speciated in several habitats. Hence, as exemplified by this model system, highly specialized permanent parasites may drastically de-specialize to the extent of becoming free-living and, thus escape from dead-end evolution. Our phylogenetic and historical ecological framework explains the limited cross-reactivity between allergens from the house dust mites and ‘storage’ mites and the ability of the dust mites to inhibit host immune responses. It also provides insights into how ancestral features related to parasitism (frequent ancestral shifts to unrelated hosts, tolerance to lower humidity, and preexisting enzymes targeting skin and keratinous materials) played a major role in reversal to the free-living state. We propose that parasitic ancestors of pyroglyphids shifted to nests of vertebrates. Later the nest-inhabiting pyroglyphids expanded into human dwellings to become a major source of allergens.

长期特化可能会限制物种响应新环境条件的能力，并提升其灭绝风险。对于永久寄生虫及其他共生生物而言，最引人关注的科学问题在于：这类生物能否重返自由生活状态，从而摆脱进化‘死胡同’的演化困境？这一问题与多洛法则（Dollo's law）直接相关，该法则明确指出，复杂性状（如自由生活与寄生生活的生活模式）无法以相同形式再次演化出现。本研究提供了确凿证据：作为一类具有重要医学意义的自由生活生物，屋尘螨（house dust mites）起源于温血脊椎动物的永久寄生虫。基于稳健的多基因系统发育拓扑结构（315个分类群、8942 nt）、祖先性状状态重建以及基于多洛法则的不可逆演化检验，研究证实屋尘螨已摒弃寄生生活模式，次生演化为自由生活生物，并随后在多种生境中发生物种分化。因此，正如本模型系统所佐证的那样，高度特化的永久寄生虫可发生大幅去特化，直至恢复自由生活状态，从而摆脱进化死胡同的演化桎梏。我们的系统发育与历史生态学框架，解释了屋尘螨与‘仓储’螨类的变应原之间交叉反应性有限的原因，以及屋尘螨抑制宿主免疫应答的能力机制。该框架还阐明了与寄生习性相关的祖先性状——包括频繁向无关宿主的宿主转换、对低湿度环境的耐受性，以及预先存在的靶向皮肤与角质物质的酶类——如何在重返自由生活状态的过程中发挥了关键作用。我们提出，嗜皮螨类（pyroglyphids）的寄生祖先曾转移至脊椎动物的巢穴中栖息；随后这些栖息于巢穴的嗜皮螨类进一步扩散至人类居所，成为主要的变应原来源。