Dioecy is associated with higher diversification rates in flowering plants

Abstract

In angiosperms, dioecious clades tend to have fewer species than their nondioecious sister clades. This departure from the expected equal species richness in the standard sister clade test has been interpreted as implying that dioecious clades diversify less and has initiated a series of studies suggesting that dioecy might be an 'evolutionary dead end'. However, two of us recently showed that the 'equal species richness' null hypothesis is not valid in the case of derived char acters, such as dioecy, and proposed a new test for sister clade comparisons; preliminary results, using a data set available in the litterature, indicated that dioecious clades migth diversify more than expected. However, it is crucial for this new test to distinguish between ancestral and derived cases of dioecy, a criterion that was not taken into account in the available data set. Here, we present a new data set that was obtained by searching the phylogenetic literature on more than 600 completely dioecious angiosperm genera and identifying 115 sister clade pairs for which dioecy is likely to be derived (including > 50% of the dioecious species). Applying the new sister clade test to this new dataset, we confirm the preliminary result that dioecy is associated with an increased diversification rate, a result that does not support the idea that dioecy is an evolutionary dead end in angiosperms. The traits usually associated with dioecy, that is, an arborescent growth form, abiotic pollination, fleshy fruits or a tropical distribution, do not influence the diversification rate. Rather than a low diversification rate, the observed species richness patterns of dioecious clades seem to be better explained by a low transition rate to dioecy and frequent losses.

Lineages ofSilene nutansdeveloped rapid, strong, asymmetric postzygotic reproductive isolation in allopatry

“…In addition, comparative genomic studies of sterilizing and nonsterilizing mitochondrial genomes that co-occur in a given species have shown that sterilizing genomes exhibit a higher rate of evolution (Darracq et al 2010(Darracq et al , 2011. As dioecy and sex-chromosomes have been suggested to drive speciation rates (Käfer et al 2014;Graves 2016), gynodioecy could reveal itself to be another reproductive system that facilitates reproductive isolation and thus speciation in a very effective way, in a tempo faster than phenotypic diversification (Orr 1995), resulting in cryptic species. Therefore, we expect that the accumulation of mutations in the mitochondrial genome occurs independently in the two S. nutans lineages and would ultimately induce reproductive isolation through cytonuclear genetic incompatibilities.…”

Macroevolutionary synthesis of flowering plant sexual systems

“…Sexual system has, however, been investigated as a possible correlate of lineage diversification rate (Heilbuth 2000;Kay et al 2006;Käfer et al 2014;Sabath et al 2016). Sexual system has, however, been investigated as a possible correlate of lineage diversification rate (Heilbuth 2000;Kay et al 2006;Käfer et al 2014;Sabath et al 2016).…”

“…Sexual system is a key determinant of genetic variation and reproductive success, affecting evolutionary processes within populations (Bawa 1980;Charlesworth and Wright 2001;Eppley and Pannell 2007;Queenborough et al 2009) and potentially the origination and extinction of species (Vamosi and Vamosi 2005;Kay et al 2006;Käfer et al 2014;Sabath et al 2016). Sexual system is a key determinant of genetic variation and reproductive success, affecting evolutionary processes within populations (Bawa 1980;Charlesworth and Wright 2001;Eppley and Pannell 2007;Queenborough et al 2009) and potentially the origination and extinction of species (Vamosi and Vamosi 2005;Kay et al 2006;Käfer et al 2014;Sabath et al 2016).…”

“…A full understanding of sexual system patterns and the processes behind them will draw on diverse functional perspectives and time scales (e.g., Renner and Ricklefs 1995;Heilbuth 2000;Diggle et al 2011;Käfer et al 2014). Population-level studies provide insight into mechanistic drivers of sex ratios and sex allocation variation (Ashman 2006;Spigler and Ashman 2011;Dufay and Billard 2012), while broad comparative analyses assess correlations with ecological factors or diversification rate (Renner and Ricklefs 1995;Heilbuth 2000;Vamosi et al 2003 Within-population processes translate into transitions among states, which can be investigated by phylogenetic studies of species-level shifts in sexual systems (e.g., Case et al 2008;Volz and Renner 2008;Schaefer and Renner 2010;Njuguna et al 2013;Rivkin et al 2016).…”

On the rarity of dioecy in flowering plants

“…First, building upon an improved test for sister clade comparisons (Käfer & Mousset ), Käfer et al . () documented a small positive effect of dioecy on species richness, suggesting that diversification might be more rapid in at least some of the dioecious lineages than in the hermaphrodite lineages from which they are derived. Second, using recently developed phylogenetic tools (Maddison et al .…”