The molecular phylogenetics of Trachymyrmex Forel ants and their fungal cultivars provide insights into the origin and coevolutionary history of 'higher-attine' ant agriculture

The molecular phylogenetics of Trachymyrmex Forel ants and their fungal cultivars provide insights into the origin and coevolutionary history of 'higher-attine' ant agriculture
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DOI:
10.1111/syen.12370
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发表时间:
2019-10-01
影响因子:
4.8
通讯作者:
Schultz, Ted R.
Schultz, Ted R.
中科院分区:
农林科学1区
文献类型:
--
作者:
Solomon, Scott E.;Rabeling, Christian;Schultz, Ted R.

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真菌生长的蚂蚁和它们的真菌品种构成了一个互惠共生的经典例子,这导致了跨越c. 55-65 Ma的复杂的共同进化动力学。在食真菌蚂蚁实践的五种农业系统中,尽管与新热带地区和北美部分地区的生态系统功能和人类农业相关,但对高氮农业(其中切叶农业是衍生子集)的了解仍然很少。在从事高海拔农业的蚂蚁中,根据目前的定义,Trachymyrmex Forel属与切叶蚁、Sericomyrmex Mayr和Xerolitor Sosa-Calvo等人拥有最近的共同祖先。虽然以前的分子系统发育研究表明,Trachymyrmex是一个副纲级,但到目前为止,分类群样本的不足阻碍了对该类群进化史的全面研究,并限制了解决其分类问题的可能性。本文采用4种核标记对38种金舌菌(49种已描述种中的27种和至少11种新种)的系统发育进行了分析,并对23种金舌菌培养的真菌进行了2种核标记的系统发育分析。获得112种蚂蚁(402个新基因序列)和95种真菌(153个新基因序列)的新基因数据。我们的结果证实了先前的发现,即目前定义的Trachymyrmex是一种过敏性疾病。我们建议承认两个新属,Mycetomoellerius属。和Paratrachymyrmex属。,并将继续使用Trachymyrmex限制在包含模式物种[Trachymyrmex septentrionalis (McCook)]的九个主要北美物种的分支中,这是切叶蚂蚁的姐妹群。我们的真菌品种系统发育总体上证实了先前观察到的抗真菌关联的广泛模式,但它也揭示了这些模式的进一步违反。高等真菌可分为两类:(i)单一种Leucoagaricus gongylophorus (Moller);(ii)其姊妹分支,由多个物种组成,最近被称为Leucoagaricus Singer“分支B”。我们的系统发育表明,尽管大多数不割叶的高氮蚂蚁通常培育B枝的物种,但一些物种培育L. gongylophorus,而另一些物种培育与低氮农业典型相关的真菌。这表明,目前由蚂蚁和真菌之间的关联所定义的农业系统并不完全符合蚂蚁和真菌的系统发育。然而,它们可能与尚不清楚的蚂蚁和/或其微生物群的生物学特性有关。
The fungus-growing ants and their fungal cultivars constitute a classic example of a mutualism that has led to complex coevolutionary dynamics spanning c. 55-65 Ma. Of the five agricultural systems practised by fungus-growing ants, higher-attine agriculture, of which leaf-cutter agriculture is a derived subset, remains poorly understood despite its relevance to ecosystem function and human agriculture across the Neotropics and parts of North America. Among the ants practising higher-attine agriculture, the genus Trachymyrmex Forel, as currently defined, shares most-recent common ancestors with both the leaf-cutter ants and the higher-attine genera Sericomyrmex Mayr and Xerolitor Sosa-Calvo et al. Although previous molecular-phylogenetic studies have suggested that Trachymyrmex is a paraphyletic grade, until now insufficient taxon sampling has prevented a full investigation of the evolutionary history of this group and limited the possibility of resolving its taxonomy. Here we describe the results of phylogenetic analyses of 38 Trachymyrmex species, including 27 of the 49 described species and at least 11 new species, using four nuclear markers, as well as phylogenetic analyses of the fungi cultivated by 23 species of Trachymyrmex using two markers. We generated new genetic data for 112 ants (402 new gene sequences) and 95 fungi (153 new gene sequences). Our results corroborate previous findings that Trachymyrmex, as currently defined, is paraphyletic. We propose recognizing two new genera, Mycetomoellerius gen.n. and Paratrachymyrmex gen.n., and restricting the continued use of Trachymyrmex to the clade of nine largely North American species that contains the type species [Trachymyrmex septentrionalis (McCook)] and that is the sister group of the leaf-cutting ants. Our fungal cultivar phylogeny generally corroborates previously observed broad patterns of ant-fungus association, but it also reveals further violations of those patterns. Higher-attine fungi are divided into two groups: (i) the single species Leucoagaricus gongylophorus (Moller); and (ii) its sister clade, consisting of multiple species, recently referred to as Leucoagaricus Singer 'clade B'. Our phylogeny indicates that, although most non-leaf-cutting higher-attine ants typically cultivate species in clade B, some species cultivate L. gongylophorus, whereas still others cultivate fungi typically associated with lower-attine agriculture. This indicates that the attine agricultural systems, which are currently defined by associations between ants and fungi, are not entirely congruent with ant and fungal phylogenies. They may, however, be correlated with as yet poorly understood biological traits of the ants and/or of their microbiomes.