Evolutionary déjà vu? A case of convergent evolution in an ant-plant association

Abstract

Obligatory ant-plant symbioses often appear to be single evolutionary shifts within particular ant lineages; however, convergence can be revealed once natural history observations are complemented with molecular phylogenetics. Here, we describe a remarkable example of convergent evolution in an ant-plant symbiotic system. Exclusively arboreal, Myrmelachista species can be generalized opportunists nesting in several plant species or obligately symbiotic, live-stem nesters of a narrow set of plant species. Instances of specialization within Myrmelachista are known from northern South America and throughout Middle America. In Middle America, a diverse radiation of specialists occupies understory treelets of lowland rainforests. The morphological and behavioural uniformity of specialists suggests that they form a monophyletic assemblage, diversifying after a single origin of specialization. Using ultraconserved element phylogenomics and ancestral state reconstructions, we show that shifts from opportunistic to obligately symbiotic evolved independently in South and Middle America. Furthermore, our analyses support a remarkable case of convergence within the Middle American radiation, with two independently evolved specialist clades, arising nearly simultaneously from putative opportunistic ancestors during the late Pliocene. This repeated evolution of a complex phenotype suggests similar mechanisms behind trait shifts from opportunists to specialists, generating further questions about the selective forces driving specialization.

Keywords: ant–plant symbioses; convergent evolution; ecological specialization; multispecies interactions; mutualism; phylogenomics.

Figure 1.

Nest detail and habitus of Myrmelachista. (a) Opportunist species (Myrmelachista zeledoni Emery, 1896) and (b) specialist species (Myrmelachista lauropacifica Longino, 2006). Figures are not to scale.

Figure 2.

Phylogeny of Myrmelachista showing the major clades and instances of obligatory symbionts. Support values on nodes indicate ultrafast bootstrap (UFB) and Shimodaira-Hasegawa-like approximate likelihood ratio test scores (SH-aLRT) and are only shown for nodes not maximally supported by both measures. Clades are colour-coded based on the legend. Taxon names are colour-coded based on nesting habits and include a unique DNA extraction code for each sample and country where the specimen was collected. Features of specialist symbionts are shown in the inset: (a) understory of Costa Rican rainforest, red circle highlighting individual of Mespilodaphne sp. (Lauraceae host plant); (b) M. lauropacifica: detail of host branch exterior (left) and excavated interior completely occupied by workers (right); (c). M. flavoguarea workers tending larvae inside the nest gallery; (d) detail of excavated cavities outside of a M. osa nest.

Figure 3.

Divergence times and evolution of nesting specialization of Myrmelachista. Numbers above nodes are mean ages in millions of years, blue bars indicate 95% HPD. Nesting habit was classified as a discrete binary character for the ancestral state reconstruction (ASR), with species either being opportunistic or specialist (=obligate symbiont). Topology shows transitions of nesting habit for Myrmelachista using a maximum-likelihood reconstruction and a stochastic character mapping approach (simmap function in the R package ‘phytools’) and the equal rates (ER) model. Transitions of character states are shown as a summary of the reconstructed changes of 1000 stochastic character histories (green and orange tones). Specialist clades are coloured based on nesting habits, as indicated in figure 2; clades are colour-coded based on the legend from figure 2.