Data from: Repeated evolution of tricellular (and bicellular) pollen

Premise of study: Male gametophytes of seed plants are sexually immature at the time they are dispersed as pollen, but approximately 30% of flowering plants have tricellular pollen containing fully formed sperm at anthesis. The classic study of Brewbaker (1967: American Journal of Botany 54: 1069–1083) provided a powerful confirmation of the long-standing hypothesis that tricellular pollen had many parallel and irreversible origins within angiosperms. We readdressed the main questions of that study with modern comparative phylogenetic methods. Methods: We used our own and more recent reports to greatly expand the Brewbaker data set. We modeled trait evolution for 2511 species on a time-calibrated angiosperm phylogeny using (1) Binary State Speciation and Extinction (BiSSE), which accounts for the effect of species diversification rates on character transition rates and, (2) the hidden rates model (HRM), which incorporates variation in transition rates across a phylogeny. Key results: Seventy percent of species had bicellular pollen. BiSSE found a 1.9-fold higher bicellular to tricellular transition rate than in the reverse direction, and bicellular lineages had a 1.8-fold higher diversification rate than tricellular lineages. HRM found heterogeneity in evolutionary rates, with bidirectional transition rates in three of four rate classes. Conclusions: The tricellular condition is not irreversible. Pollen cell numbers are maintained at intermediate frequencies because lower net diversification rates of tricellular lineages are counterbalanced by slower state shifts to the bicellular condition. That tricellular lineages diversify slowly and give rise to bicellular lineages slowly reflects a linkage between the evolution of sporophyte lifestyles and the developmental lability of male gametophytes.

研究背景：种子植物的雄配子体（male gametophytes）在以花粉形式散播时仍处于性未成熟状态，但约30%的被子植物（angiosperms）在开花期（anthesis）时拥有包含完全成熟精子的三细胞花粉（tricellular pollen）。Brewbaker（1967年，《美国植物学杂志》54卷：1069–1083）的经典研究有力证实了长期存在的假说：三细胞花粉在被子植物中存在多次平行且不可逆转的起源。本研究借助现代比较系统发育方法，重新探讨了该经典研究的核心问题。研究方法：本研究结合自身及近年发表的相关报告，大幅扩充了Brewbaker的数据集。我们基于一棵经过时间校准的被子植物系统发育树，对2511个物种的性状演化进行建模，分别采用了两种分析方法：(1) 二元状态物种形成与灭绝模型（Binary State Speciation and Extinction，BiSSE），该模型可考量物种分化速率对性状转换速率的影响；(2) 隐速率模型（hidden rates model，HRM），该模型纳入了系统发育树中不同分支的性状转换速率差异。主要结果：70%的物种拥有二细胞花粉（bicellular pollen）。BiSSE分析显示，二细胞花粉向三细胞花粉的转换速率是反向转换速率的1.9倍，且二细胞花粉演化支的分化速率是三细胞花粉演化支的1.8倍。HRM分析则发现演化速率存在异质性，四个速率类别中有三类呈现双向的性状转换。研究结论：三细胞花粉的演化状态并非不可逆转。花粉细胞数量维持在中间频率，是因为三细胞花粉演化支较低的净分化速率，与向二细胞花粉状态转换的较慢速率相互抵消。三细胞花粉演化支分化缓慢且向二细胞花粉演化支转换的速率同样较慢，这一现象反映了孢子体生活型的演化与雄配子体发育可塑性之间的关联。