Correlated evolution of senescence and ephemeral substrate use in the Sordariomycetes

Evolutionary theory predicts that senescence – a decline in reproduction and survival with increasing age - can evolve as a trade-off between the investment in reproduction on one side and in somatic maintenance and repair on the other side. The ecology of a species is crucial here, since it provides the external causes of death that determine the statistical limit to a species’ lifespan. Filamentous fungi are generally believed to be non-senescent, and there are indeed spectacular examples of very old fungal individuals in nature. Yet, for some fungi the growth conditions are ephemeral and therefore senescence is expected to have evolved, like in the coprophilic Podospora anserina, the only well-studied filamentous fungus with intrinsic senescence. Here we hypothesize that rapid senescence is more common in fungi than generally believed and that the phylogenetic distribution of senescence correlates with its ecology. We examined a set of Sordariomycetes for their lifespan and constructed phylogenies based on several nuclear sequences. Part of the strains were from the CBS culture collection, originally isolated from various substrates, some of which ephemeral. In addition we isolated new strains from short-lived substrates. Senescence was observed throughout the phylogeny. Correlation tests support the hypothesis that in the Sordariomycetes senescence is a trait that has arisen as an evolved adaptation to ephemeral substrates, and that it has evolved repeatedly and independently along the phylogeny.

进化理论预测，衰老（senescence）——即随年龄增长而出现的繁殖与生存能力下降——能够演化形成，其本质是繁殖投入与体细胞维护修复投入之间的权衡。物种的生态环境在此至关重要，因为它提供了决定物种寿命统计上限的外部死亡因素。丝状真菌（filamentous fungi）通常被认为不会发生衰老，自然界中也确实存在诸多寿命极长的真菌个体的典型案例。然而，部分真菌的生长环境短暂易逝，因此这类真菌有望演化出衰老特性，比如嗜粪的小白鼠粪生柄孢壳（Podospora anserina）——这是目前唯一被充分研究的具有内在衰老特性的丝状真菌。本研究提出假说：真菌中快速衰老的现象远比此前认知的更为普遍，且衰老的系统发育分布与其生态环境存在相关性。我们选取了一批粪壳菌纲（Sordariomycetes）物种检测其寿命，并基于多个核基因序列构建了系统发育树。部分菌株取自CBS菌种保藏中心（CBS culture collection），这些菌株最初分离自多种基质，其中部分基质的存续周期较短。此外，我们还从存续周期较短的基质中分离得到了新的菌株。研究在整个系统发育分支中均观察到了衰老现象。相关性检验验证了本研究的假说：在粪壳菌纲中，衰老是一种演化而来的、适应短暂基质环境的性状，且该性状在系统发育过程中多次独立演化产生。