Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA.
J Evol Biol. 2018 Dec;31(12):1863-1875. doi: 10.1111/jeb.13381. Epub 2018 Oct 31.
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.
特征多次出现但仍然罕见，这呈现出一种奇特的悖论。这些罕见特征中的许多都表现出明显的尖端模式，它们在系统发育中广泛分布，与短分支相关，并且在最近分化的姐妹物种之间存在差异。这种系统发育模式传统上归因于特征是进化的死胡同，特征是由于某种短期进化优势而出现的，但最终导致物种灭绝。虽然与死胡同特征相关的更高灭绝率可能会产生这种尖端模式，但如果具有该特征的谱系比其他谱系进化得更慢，或者如果该特征更容易丢失而不是获得，那么也可能会出现类似的模式。在这项研究中，我们量化了番茄科茄属植物中红花的尖端程度，并研究了可以解释该特征稀疏系统发育分布的宏观进化过程。使用一系列指标，我们确认红花谱系在整个树上明显过度分散，并且形成的小分支比在零模型下预期的要小。接下来，我们使用 HiSSE（隐藏状态物种形成和灭绝）拟合 22 个替代模型，该模型可以适应取决于观察到和未观察到（隐藏）特征状态的物种形成、灭绝和转换率的不对称性。模型拟合的结果表明，该家族的多样化率存在显著差异，这可以通过包含隐藏状态来很好地解释。我们的最佳拟合模型在最大枝聚类可信度树和包含系统发育不确定性时有所不同，这表明红花茄科植物的极端尖端和罕见性使得很难区分不同的潜在过程。然而，两个最佳模型都强烈支持红花丢失的偏见。当包含系统发育不确定性时，拟合度最高的 HiSSE 模型为这样一种假设提供了一些支持，即具有红花的谱系由于灭绝率升高而表现出降低的多样化率。未来的研究通过模拟或针对种群水平的过程，可能使我们能够确定茄科或其他被子植物类群的红花是否由于多种过程的组合或不对称的转变而罕见且尖端。
