Why are red flowers so rare? Testing the macroevolutionary causes of tippiness

Abstract

Traits that have arisen multiple times yet still remain rare present a curious paradox. A number of these rare traits show a distinct tippy pattern, where they appear widely dispersed across a phylogeny, are associated with short branches and differ between recently diverged sister species. This phylogenetic pattern has classically been attributed to the trait being an evolutionary dead end, where the trait arises due to some short‐term evolutionary advantage, but it ultimately leads species to extinction. While the higher extinction rate associated with a dead end trait could produce such a tippy pattern, a similar pattern could appear if lineages with the trait speciated slower than other lineages, or if the trait was lost more often that it was gained. In this study, we quantify the degree of tippiness of red flowers in the tomato family, Solanaceae, and investigate the macroevolutionary processes that could explain the sparse phylogenetic distribution of this trait. Using a suite of metrics, we confirm that red‐flowered lineages are significantly overdispersed across the tree and form smaller clades than expected under a null model. Next, we fit 22 alternative models using HiSSE (Hidden State Speciation and Extinction), which accommodates asymmetries in speciation, extinction and transition rates that depend on observed and unobserved (hidden) character states. Results of the model fitting indicated significant variation in diversification rates across the family, which is best explained by the inclusion of hidden states. Our best fitting model differs between the maximum clade credibility tree and when incorporating phylogenetic uncertainty, suggesting that the extreme tippiness and rarity of red Solanaceae flowers makes it difficult to distinguish among different underlying processes. However, both of the best models strongly support a bias towards the loss of red flowers. The best fitting HiSSE model when incorporating phylogenetic uncertainty lends some support to the hypothesis that lineages with red flowers exhibit reduced diversification rates due to elevated extinction rates. Future studies employing simulations or targeting population‐level processes may allow us to determine whether red flowers in Solanaceae or other angiosperms clades are rare and tippy due to a combination of processes, or asymmetrical transitions alone.

Adaptation to hummingbird pollination is associated with reduced diversification inPenstemon

“…Other examples include the evolution of host specialization in bark beetles, the evolution of sociality in spiders, and the evolution of asexuality (Kelley and Farrell 1998;Agnarsson et al 2006;Schwander and Crespi 2009). This pattern of rarity despite high rates of transition to the derived state can lead to a phylogenetic pattern of "tippiness," as well documented for certain transitions in flower color (Ng and Smith 2018).…”

“…; Schwander and Crespi ). This pattern of rarity despite high rates of transition to the derived state can lead to a phylogenetic pattern of “tippiness,” as well documented for certain transitions in flower color (Ng and Smith ).…”

All the Colors of the Rainbow: Diversification of Flower Color and Intraspecific Color Variation in the Genus Iris

“…The diversity of flower color among and within these modern lineages suggests that most of these transitions must have been adaptive ( Rausher, 2008 ). While the mutations causing flower color shifts are well understood at the biochemical level ( Grotewold, 2006 ), the broader macro-evolutionary drivers of flower color diversity have only been studied in few plant groups ( Landis et al, 2018 ; Ng and Smith, 2018 ). To understand these macro-evolutionary forces, we need to explore plant lineages exhibiting a diversity of flower colors.…”

Macroevolutionary and macroecological approaches to understanding the evolution of stress tolerance in plants

“…For example, some cases of tippy distribution of pollinator specialisation have been interpreted as a sign of decreased speciation rate. Cases have been identified where lineages with moth pollinated flowers, self-pollinated flowers or red flowers appear not to diversify at the same rate as other species, so on the phylogeny they occur as "lonely species" rather than in clades of species all sharing the same pollination syndrome or flower type (Day et al, 2016;Gamisch, Fischer, & Comes, 2015;Ng & Smith, 2018;Tripp & Manos, 2008). A similar argument has been made for the tippy distribution of asexuality, especially in animals, where it arises often but rarely gives rise to long-lived clonal species, nor to diverse clades of asexually reproducing species (Schwander & Crespi, 2008).…”

“…There are several possible measures of the tippiness of a trait (Agnarsson, Avilés, Coddington, & Maddison, 2006;Bromham et al, 2016;Ng & Smith, 2018;Schwander & Crespi, 2008). The simplest and most effective is the number of species per origin, that is, the number of species with the trait divided by the number of inferred origins.…”