Climate outweighs native vs. non-native range-effects for genetics and common garden performance of a cosmopolitan weed

Comparing genetic diversity, genetic differentiation and performance between native and non-native populations has advanced our knowledge of contemporary evolution and its ecological consequences. However, such between-range comparisons can be complicated by high among-population variation within native and non-native ranges. For example, native vs. non-native comparisons between small and non-representative subsets of populations for species with very large distributions have the potential to mislead because they may not sufficiently account for within-range adaptation to climatic conditions, and demographic history that may lead to non-adaptive evolution. We used the cosmopolitan weed Conyza canadensis to study the interplay of adaptive and demographic processes across, to our knowledge, the broadest climatic gradient yet investigated in this context. To examine the distribution of genetic diversity, we genotyped 26 native and 26 non-native populations at 12 microsatellite loci. Furthermore, we recorded performance traits for 12 native and 13 non-native populations in the field and in the common garden. To analyze how performance was related to range and/or climate, we fit pedigree mixed-effects models. These models weighed the population random effect for co-ancestry to account for the influence of demographic history on phenotypic among-population differentiation. Genetic diversity was very low, selfing rates were very high, and both were comparable between native and non-native ranges. Non-native populations out-performed native populations in the field. However, our most salient result was that both neutral genetic differentiation and common garden performance were far more correlated with the climatic conditions from which populations originated than native vs. non-native range-affiliation. Including co-ancestry of our populations in our models greatly increased explained variance and our ability to detect significant main effects for among-population variation in performance. High propagule pressure and high selfing rates, in concert with the ability to adapt rapidly to climatic gradients, may have facilitated the global success of this weed. Neither native nor non-native populations were homogeneous groups but responded comparably to similar environments in each range. We suggest that studies of contemporary evolution should consider widely distributed and genotyped populations to disentangle native vs. non-native range-effects from varying adaptive processes within ranges and from potentially confounding effects of demographic history.

对比本土种群与外来种群的遗传多样性、遗传分化及表现型表现，可深化我们对当代演化及其生态效应的认知。然而，本土与外来分布区内种群间的高变异程度，会使这类分布区间对比研究变得复杂。例如，对于分布范围极广的物种，若仅选取少量且不具代表性的种群开展本土与外来种群对比，研究结果可能产生误导——这类研究未能充分考量分布区内种群对气候条件的适应，以及可能引发非适应性演化的种群历史动态。本研究以广布性杂草加拿大蓬（Conyza canadensis）为对象，探究适应性演化与种群历史动态间的相互作用；据我们所知，这是该研究方向中覆盖气候梯度最广的一次尝试。为解析遗传多样性的分布格局，我们对26个本土种群与26个外来种群的12个微卫星位点（microsatellite loci）进行了基因分型。此外，我们在野外与同质园（common garden）试验中，记录了12个本土种群与13个外来种群的表现型性状。为解析表现型表现与分布区间及/或气候的关联，我们采用了谱系混合效应模型（pedigree mixed-effects models）进行拟合。此类模型通过考量种群共祖关系的随机效应，以控制种群历史动态对种群间表型分化的影响。研究发现，遗传多样性水平极低，自交率（selfing rates）极高，且本土与外来分布区间的这两项指标并无显著差异。野外环境下，外来种群的表现优于本土种群。然而，本研究最显著的结果是：相较于本土与外来分布区间的归属，中性遗传分化与同质园试验中的表现型表现，均与种群起源地的气候条件关联更为紧密。在模型中纳入种群共祖关系后，模型可解释的方差大幅提升，同时我们也更易检测到种群间表现型变异的显著主效应。高繁殖体压力（propagule pressure）与高自交率，配合种群快速适应气候梯度的能力，或许共同推动了该杂草在全球范围内的成功定植与扩散。本土与外来种群均并非均质类群，但二者在各自分布区内对相似环境的响应模式并无显著差异。我们建议，当代演化相关研究应选取分布广泛且完成基因分型的种群，以区分本土与外来分布区间的效应、分布区内多样的适应性演化过程，以及可能造成混淆的种群历史动态效应。