Disentangling the Effects of Key Innovations on the Diversification of Bromelioideae (Bromeliaceae)

Abstract

The evolution of key innovations, novel traits that promote diversification, is often seen as major driver for the unequal distribution of species richness within the tree of life. In this study, we aim to determine the factors underlying the extraordinary radiation of the subfamily Bromelioideae, one of the most diverse clades among the neotropical plant family Bromeliaceae.Based on an extended molecular phylogenetic data set, we examine the effect of two putative key innovations, that is, the Crassulacean acid metabolism (CAM) and the water-impounding tank, on speciation and extinction rates. To this aim, we develop a novel Bayesian implementation of the phylogenetic comparative method, binary state speciation and extinction, which enables hypotheses testing by Bayes factors and accommodates the uncertainty on model selection by Bayesian model averaging. Both CAM and tank habit were found to correlate with increased net diversification, thus fulfilling the criteria for key innovations. Our analyses further revealed that CAM photosynthesis is correlated with a twofold increase in speciation rate, whereas the evolution of the tank had primarily an effect on extinction rates that were found five times lower in tank-forming lineages compared to tank-less clades. These differences are discussed in the light of biogeography, ecology, and past climate change. K E Y W O R D S :BiSSE-BMA, key innovation, macroevolution, speciation extinction rates.

Morphological Phylogenetic Analysis of Two Early-Diverging Genera of Bromelioideae (Bromeliaceae)

“…All the phylogenies that have included more than one species of Bromelia have indicated that the genus is monophyletic (e.g., Schulte & Zizka 2008;Sass & Spech 2010;Silvestro et al 2014;Evans et al 2015). However, the monophyly of Bromelia was not confirmed in the present analysis, because of the positioning of B. irwinii.…”

“…Nevertheless, these factors might have been strong forces driving the speciation and the evolutionary success of Bromelia in the Cerrado. Similarly, the repeated expansions and contractions of the Atlantic Rainforest and Cerrado during the Pleistocene (Pennington et al 2004;Antonelli et al 2009;Antonelli & Sanmartin 2011;Silvestro et al 2014) may have affected the occupation of Bromelia and its speciation in the Atlantic Rainforest (Bromelia antiacantha, B. unaensis and B. binotii). Probably it is also the key for the migration of members of Bromelioideae from arid environments to the evergreen forest, the present diversity center for this subfamily (Martinelli et al 2008;Forzza et al 2014).…”

“…The increased speciation rate could be associated with the water saving CAM physiology and the low competition for the niches, since they occupy sites in which plants with no adaptations for dry environments can not be established (Benzing 2000;Givnish et al 2014;Silvestro et al 2014).…”

Canistropsis e Nidularium (Bromeliaceae: Bromelioideae) no Parque Nacional da Serra dos Órgãos, Rio de Janeiro, Brasil

“…Entre as oito subfamílias reconhecidas atualmente (Givnish et al 2007(Givnish et al , 2011, Bromelioideae é aquela com maiores problemas de delimitação genérica e cujos conceitos taxonômicos são claramente divergentes entre os diferentes tratamentos (e.g., Baker 1889; Mez 1896Mez , 1934Smith & Downs 1979). A maioria das hipóteses filogenéticas propostas até o presente converge para o monofiletismo da subfamília e para o reconhecimento de um clado eu-bromelioide com a maioria dos gêneros (e.g., Schulte et al 2009;Sass & Specht 2010;Givnish et al 2011;Silvestro et al 2014;Evans et al 2015). O clado nidularióide, tem sido reconhecido em diferentes análises, porém ainda subamostrado e com relacionamentos inconclusivos (Schulte et al 2009;Evans et al 2015).…”

From species to trait evolution in Aethionema (Brassicaceae)

“…Examples of such studies have been conducted within the Bromelioideae and Solanaceae. In Bromelioideae CAM photosynthesis correlated to net speciation, while the tank habit correlates with extinction (Silvestro et al 2014). Within Solanaceae core group self-incompatibility seems to drive speciation (Goldberg et al 2010).…”