Macroevolutionary dynamics in the transition of angiosperms to aquatic environments

Abstract

Angiosperm lineages in aquatic environments are characterized by high structural and functional diversity, and wide distributions. A long-standing evolutionary riddle is what processes have caused the relatively low diversity of aquatic angiosperms compared to their terrestrial relatives.We use diversification and ancestral reconstruction models with a comprehensive > 10 000 genus angiosperm phylogeny to elucidate the macroevolutionary dynamics associated with transitions of terrestrial plants to water.Our study reveals that net diversification rates are significantly lower in aquatic than in terrestrial angiosperms due to lower speciation and higher extinction. Shifts from land to water started early in angiosperm evolution, but most events were concentrated during the last c. 25 million years. Reversals to a terrestrial habitat started only 40 million years ago, but occurred at much higher rates. Within aquatic angiosperms, the estimated pattern is one of gradual accumulation of lineages, and relatively low and constant diversification rates throughout the Cenozoic.Low diversification rates, together with infrequent water transitions, account for the low diversity of aquatic angiosperms today. The stressful conditions and small global surface of the aquatic habitat available for angiosperms are hypothesized to explain this pattern.

Allometric relationships between leaf and petiole traits across 31 floating-leaved plants reveal a different adaptation pattern from terrestrial plants

“…However, there may still be another possibility that aquatic plants keep similar allometric relationships to their terrestrial relatives, because aquatic angiosperms have undergone hundreds of events of plant ‘regression’ evolution from terrestrial ancestors ( Sculthorpe, 1967 ; Cook, 1988 ; Les, 2015 ; Meseguer et al , 2022 ), probably leading to a high phylogenetic conservatism in stomata and petiole traits of aquatic plants and similar allometric relationships to their terrestrial relatives ( Liu et al , 2015 ; Chen et al , 2022 ). Thus, comparative analyses on the allometric scaling across species should consider phylogeny, and we do not know whether the allometric scaling between leaf stomata and petiole xylem traits of floating-leaved plants still exist despite the different phylogenetic backgrounds.…”

Widespread evolution of poricidal flowers: A striking example of morphological convergence across flowering plants

“…The Smith and Brown (2018) tree was primarily created using mega tree methodology, that is, matching different large angiosperm phylogenies to generate a larger and more complete tree for genus-level data, but cannot be used for species-level data due to lack of resolution at that level. Therefore, for the angiosperm wide genus-level analysis, we pruned the tree to one species per genus (for a similar approach see Meseguer et al ., 2022). The second tree we used was the Meseguer et al (2022) genus level-phylogeny, also created from the Smith and Brown (2018) tree.…”

“…However, we noted that when we pruned the Smith and Brown (2018) phylogeny we had to resolve polytomies in the genus-level tree, and we did this at random using the function multid2di() in R package ape (Paradis et al, 2004). This is an important detail, because the algorithm used to resolve polytomies might change the estimation of diversification rates, and this is the main difference between the Meseguer et al 2022 and our pruned tree. For both genus-level phylogenies we matched a total of 10,328 genera.…”

“…For the two other families analyzed at the species level (Melastomataceae and Fabaceae), models did not converge after running the analyses for several months due to high uncertainty on the branch lengths in the Melastomataceae and Fabaceae trees and thus we lack results for these groups (additional discussion in Supporting Information). Using the Meseguer et al (2022) phylogeny, we found that poricidal states have faster net diversification for poricidal in states A and B (Supporting Information Fig. S2).…”

“…We therefore conducted an extensive literature survey to identify all presently known angiosperm genera containing species with poricidal flowers. We then used an angiosperm-wide phylogeny at the genus level (as recently done in Meseguer et al ., 2022) to determine the phylogenetic distribution of poricidal flowers, the geologic ages of poricidal lineages, and the number of independent gains and losses of functionally poricidal floral morphology before the origination of genera. We also conducted diversification rate analyses at the species level to estimate if the evolution of poricidal flowers is associated with changes in speciation/extinction.…”