Accelerated diversification correlated with functional traits shapes extant diversity of the early divergent angiosperm family Annonaceae

Abstract

Background A major goal of phylogenetic systematics is to understand both the patterns of diversification and the processes by which these patterns are formed. Few studies have focused on the ancient, species-rich Magnoliales clade and its diversification pattern. Within Magnoliales, the pantropically distributed Annonaceae are by far the most genus-rich and species-rich family-level clade, with c. 110 genera and c. 2,400 species. We investigated the diversification patterns across Annonaceae and identified traits that show varied associations with diversification rates using a time-calibrated phylogeny of 835 species (34.6% sampling) and 11,211 aligned bases from eight regions of the plastid genome (rbcL, matK, ndhF, psbA-trnH, trnL-F, atpB-rbcL, trnS-G, and ycf1). Two hypotheses that might explain patterns of diversification—the ‘museum model’ and heterogeneous diversification rates—are also evaluated. Results Twelve rate shifts were identified using BAMM: in Annona, Artabotrys, Asimina, Drepananthus, Duguetia, Goniothalamus, Guatteria, Uvaria, Xylopia, the tribes Miliuseae and Malmeeae, and the Desmos-Dasymaschalon-Friesodielsia-Monanthotaxis clade (which collectively account for over 80% of the total species richness in the family). TurboMEDUSA and method-of-moments estimator analyses showed largely congruent results. A positive relationship between species richness and diversification rate is revealed using PGLS. We further explore the possible role of selected traits (habit, pollinator trapping, floral sex expression, pollen dispersal unit, anther septation, and seed dispersal unit) in shaping diversification patterns, based on inferences of BiSSE, MuSSE, HiSSE, and FiSSE analyses. Our results suggest that the liana habit, the presence of circadian pollinator trapping, androdioecy, and the dispersal of seeds as single-seeded monocarp fragments are closely correlated with higher diversification rates; pollen aggregation and anther septation, in contrast, are associated with lower diversification rates. Conclusion Our results show that the high species richness in Annonaceae is likely the result of recent increased diversification rather than the steady accumulation of species via the ‘museum model’. BAMM, turboMEDUSA, and the method-of-moments estimator all indicate heterogeneity in diversification rates across the phylogeny, with different traits associated with shifts in diversification rates in different Annonaceae clades.

Comparative analysis of plastid genomes reveals rearrangements, repetitive sequence features, and phylogeny in the Annonaceae

“…Unlike the massive expansion of IR regions, IR regions are sometimes lost ( Ruhlman et al., 2017 ; Cauz-Santos et al., 2020 ) or contracted ( He et al., 2020 ) in the plastomes of some plant lineages and algae. Previous studies have shown that many characteristics in Annonaceae are closely associated with its high diversification rate, such as climbing habits, day-night rhythm of pollen adhesion, monoecy, and seed dispersal with seeds enclosed in single-seeded fruits ( Xue et al., 2019 ). We observed three different arrangement patterns in the plastomes of seven species within the Annona , demonstrating the diversity of plastome structures within this genus.…”

Climatic and biogeographic processes underlying the diversification of the pantropical flowering plant family Annonaceae

“…The family Annonaceae (Magnoliales) represents a study model for understanding the macroevolution of tropical forests. The family originated in the early Cretaceous (112.6-89 Ma;Xue et al, 2020). It is a large and highly diverse pantropical lineage, comprising approximately 2440 species, widely distributed in tropical lowland forests (Couvreur et al, 2012).…”

“…A previous study (Couvreur et al, 2011) has suggested that lineages within Annonaceae accumulated through stable diversification rates over time, although the limited taxon sampling (4.8% of species) is likely to have resulted in an underestimation of diversification rate. More recent research (Xue et al, 2020) with improved sampling (34.2% of species) proposes an accelerated diversification in Annonaceae around 25 Ma. Certain biotic factors in Annonaceae, such as pollinator trapping, androdioecy, and single-seeded monocarp fragments, are possibly correlated with high diversification rates (Xue et al, 2020).…”

“…More recent research (Xue et al, 2020) with improved sampling (34.2% of species) proposes an accelerated diversification in Annonaceae around 25 Ma. Certain biotic factors in Annonaceae, such as pollinator trapping, androdioecy, and single-seeded monocarp fragments, are possibly correlated with high diversification rates (Xue et al, 2020). The contribution of biogeography and climate change to the rapid diversification rate increase has yet to be investigated, however.…”

“…Key opportunities here represent lineages migrating to a new region that provides a similar environment (Moore and Donoghue, 2007), and key innovations here refer to the climatic niche resulting from innovations in intrinsic traits. Other localized opportunities, such as changing climates in situ following the uplift of mountains, and morphological trait innovations explored by Xue et al (2020), are not considered in this study. In a recent study by Wang et al (2021), a correlation was revealed between the rate of climate niche evolution and high diversification rate in Annonaceae.…”