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尚未完成有性发育，但约30%的被子植物（angiosperms）在开花期（anthesis）会产生携带完全成熟精子的三细胞花粉（tricellular pollen）。布鲁贝克（Brewbaker）1967年发表于《美国植物学杂志》（American Journal of Botany）第54卷1069–1083页的经典研究，为“三细胞花粉在被子植物中存在多次平行且不可逆起源”这一长期假说提供了有力佐证。本研究采用现代比较系统发育学方法，重新探讨了该经典研究的核心问题。 研究方法：我们整合自有数据与近年发表的研究成果，极大拓展了布鲁贝克的数据集。基于经过时间校准的被子植物系统发育树（angiosperm phylogeny），我们对2511个物种的性状演化开展建模分析，采用两种模型：（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），该模型可纳入系统发育树不同分支间的转换速率变异。 关键结果：70%的物种携带二细胞花粉（bicellular pollen）。二元状态物种形成与灭绝模型（BiSSE）结果显示，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较三细胞花粉演化支高出1.8倍。隐速率模型（HRM）结果显示演化速率存在异质性，四个速率类别中有三类均存在双向的性状转换速率。 研究结论：三细胞花粉的演化状态并非不可逆。花粉细胞数量维持在中间频率，是由于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二者相互抵消。三细胞花粉演化支分化缓慢且向二细胞花粉演化支的转换速率较低，这一现象反映了孢子体（sporophyte）生活史演化与雄配子体发育可塑性之间的内在关联。