A mistletoe tale: postglacial invasion of Psittacanthus schiedeanus (Loranthaceae) to Mesoamerican cloud forests revealed by molecular data and species distribution modeling

Background: Ecological adaptation to host taxa is thought to result in mistletoe speciation via race formation. However, historical and ecological factors could also contribute to explain genetic structuring particularly when mistletoe host races are distributed allopatrically. Using sequence data from nuclear (ITS) and chloroplast (trnL-F) DNA, we investigate the genetic differentiation of 31 Psittacanthus schiedeanus (Loranthaceae) populations across the Mesoamerican species range. We conducted phylogenetic, population and spatial genetic analyses on 274 individuals of P. schiedeanus to gain insight of the evolutionary history of these populations. Species distribution modeling, isolation with migration and Bayesian inference methods were used to infer the evolutionary transition of mistletoe invasion, in which evolutionary scenarios were compared through posterior probabilities. Results: Our analyses revealed shallow levels of population structure with three genetic groups present across the sample area. Nine haplotypes were identified after sequencing the trnL-F intergenic spacer. These haplotypes showed phylogeographic structure, with three groups with restricted gene flow corresponding to the distribution of individuals/populations separated by habitat (cloud forest localities from San Luis Potosí to northwestern Oaxaca and Chiapas, localities with xeric vegetation in central Oaxaca, and localities with tropical deciduous forests in Chiapas), with post-glacial population expansions and potentially corresponding to post-glacial invasion types. Similarly, 44 ITS ribotypes suggest phylogeographic structure, despite the fact that most frequent ribotypes are widespread indicating effective nuclear gene flow via pollen. Gene flow estimates, a significant genetic signal of demographic expansion, and range shifts under past climatic conditions predicted by species distribution modeling suggest post-glacial invasion of P. schiedeanus mistletoes to cloud forests. However, Approximate Bayesian Computation (ABC) analyses strongly supported a scenario of simultaneous divergence among the three groups isolated recently. Conclusions: Our results provide support for the predominant role of isolation and environmental factors in driving genetic differentiation of Mesoamerican parrot-flower mistletoes. The ABC results are consistent with a scenario of post-glacial mistletoe invasion, independent of host identity, and that habitat types recently isolated P. schiedeanus populations, accumulating slight phenotypic differences among genetic groups due to recent migration across habitats. Under this scenario, climatic fluctuations throughout the Pleistocene would have altered the distribution of suitable habitat for mistletoes throughout Mesoamerica leading to variation in population continuity and isolation. Our findings add to an understanding of the role of recent isolation and colonization in shaping cloud forest communities in the region.

研究背景：学界普遍认为，对寄主类群的生态适应会通过宗群形成驱动槲寄生（mistletoe）的物种形成。然而，历史与生态因素同样可能解释其遗传结构的形成，尤其当槲寄生寄主宗群呈异域分布时。本研究依托核基因组内转录间隔区（ITS, internal transcribed spacer）与叶绿体trnL-F基因间隔区的序列数据，针对分布于中美洲物种分布范围内的31个施氏鹦鹉花寄生（*Psittacanthus schiedeanus*，桑寄生科Loranthaceae）种群开展遗传分化分析。我们对274株施氏鹦鹉花寄生个体进行了系统发育、种群遗传学与空间遗传分析，以解析该类群的进化历史。此外，结合物种分布模型、隔离与迁移（isolation with migration）分析与贝叶斯推断方法，我们对槲寄生入侵的进化过渡场景进行了推断，并通过后验概率比较不同进化假说。
研究结果：本研究分析显示种群遗传结构较浅，采样区域内共存在3个遗传类群。对trnL-F基因间隔区测序后共鉴定出9个单倍型，这些单倍型呈现明显的系统地理结构：3个基因流受限的类群分别对应受生境隔离的个体/种群分布格局——即从圣路易斯波托西至瓦哈卡西北部与恰帕斯的云雾林生境、瓦哈卡中部的旱生植被生境，以及恰帕斯的热带落叶林生境；上述类群均存在冰后种群扩张事件，且可能对应冰后入侵类型。同理，44个ITS核糖体基因型（ribotypes）同样呈现系统地理结构，尽管多数高频核糖体基因型分布广泛，表明通过花粉实现的核基因流较为高效。基因流估算结果、显著的种群扩张遗传信号，以及物种分布模型预测的过去气候条件下的分布范围变化，均表明施氏鹦鹉花寄生在冰后期入侵至云雾林生境。不过，近似贝叶斯计算（Approximate Bayesian Computation, ABC）分析强烈支持这3个类群在近期发生同时趋异分化的场景。
研究结论：本研究结果支持隔离与环境因素是驱动中美洲鹦鹉花寄生遗传分化的主要因素。近似贝叶斯计算分析结果与"冰后期槲寄生入侵"假说一致，该过程不受寄主种类影响；且生境类型近期隔离了施氏鹦鹉花寄生种群，由于跨生境的近期基因流，不同遗传类群间仅积累了轻微的表型差异。根据该假说，更新世时期的气候波动改变了中美洲全境适宜槲寄生生存的生境分布，进而导致种群连续性与隔离状态出现变化。本研究结果有助于进一步理解近期隔离与定殖过程对该区域云雾林群落结构的塑造作用。