Miller Jill S, Levin Rachel A, Feliciano Natalie M
Department of Biology, Amherst College, Amherst, MA 01002, USA.
Evolution. 2008 May;62(5):1052-65. doi: 10.1111/j.1558-5646.2008.00358.x. Epub 2008 Mar 1.
Over 50 years ago, Baker (1955, 1967) suggested that self-compatible species were more likely than self-incompatible species to establish new populations on oceanic islands. His logic was straightforward and rested on the assumption that colonization was infrequent; thus, mate limitation favored the establishment of self-fertilizing individuals. In support of Baker's rule, many authors have documented high frequencies of self-compatibility on islands, and recent work has solidified the generality of Baker's ideas. The genus Lycium (Solanaceae) has ca. 80 species distributed worldwide, and phylogenetic studies suggest that Lycium originated in South America and dispersed to the Old World a single time. Previous analyses of the S-RNase gene, which controls the stylar component of self-incompatibility, have shown that gametophytically controlled self-incompatibility is ancestral within the genus, making Lycium a good model for investigating Baker's assertions concerning reproductive assurance following oceanic dispersal. Lycium is also useful for investigations of reproductive evolution, given that species vary both in sexual expression and the presence of self-incompatibility. A model for the evolution of gender dimorphism suggests that polyploidy breaks down self-incompatibility, leading to the evolution of gender dimorphism, which arises as an alternative outcrossing mechanism. There is a perfect association of dimorphic gender expression, polyploidy, and self-compatibility (vs. cosexuality, diploidy, and self-incompatibility) among North American Lycium. Although the association between ploidy level and gender expression also holds for African Lycium, to date no studies of mating systems have been initiated in Old World species. Here, using controlled pollinations, we document strong self-incompatibility in two cosexual, diploid species of African Lycium. Further, we sequence the S-RNase gene in 15 individuals from five cosexual, diploid species of African Lycium and recover 24 putative alleles. Genealogical analyses indicate reduced trans-generic diversity of S-RNases in the Old World compared to the New World. We suggest that genetic diversity at this locus was reduced as a result of a founder event, but, despite the bottleneck, self-incompatibility was maintained in the Old World. Maximum-likelihood analyses of codon substitution patterns indicate that positive Darwinian selection has been relatively strong in the Old World, suggesting the rediversification of S-RNases following a bottleneck. The present data thus provide a dramatic exception to Baker's rule, in addition to supporting a key assumption of the Miller and Venable (2000) model, namely that self-incompatibility is associated with diploidy and cosexuality.
50多年前，贝克（1955年、1967年）提出，自交亲和物种比自交不亲和物种更有可能在海洋岛屿上建立新种群。他的逻辑很简单，基于这样一个假设：定殖很少发生；因此，配偶限制有利于自花受精个体的建立。为支持贝克法则，许多作者记录了岛屿上自交亲和的高频率现象，最近的研究巩固了贝克观点的普遍性。枸杞属（茄科）约有80个物种分布于全球，系统发育研究表明枸杞起源于南美洲，并仅一次扩散到旧世界。先前对控制自交不亲和花柱成分的S-RNase基因的分析表明，配子体控制的自交不亲和是该属的祖先特征，这使得枸杞成为研究贝克关于海洋扩散后生殖保障断言的良好模型。鉴于枸杞属物种在性表达和自交不亲和的存在方面存在差异，它也有助于生殖进化的研究。一个性别二态性进化模型表明，多倍体打破了自交不亲和，导致性别二态性的进化，这是作为一种替代的异交机制出现的。在北美枸杞中，二态性性别表达、多倍体和自交亲和（相对于雌雄同体、二倍体和自交不亲和）之间存在完美关联。尽管倍性水平与性别表达之间的关联在非洲枸杞中也成立，但迄今为止尚未对旧世界物种开展交配系统的研究。在这里，通过控制授粉，我们记录了非洲枸杞两个雌雄同体二倍体物种中强烈的自交不亲和现象。此外，我们对来自非洲枸杞五个雌雄同体二倍体物种的15个个体的S-RNase基因进行了测序，并获得了24个推定等位基因。系统发育分析表明，与新世界相比，旧世界S-RNases的跨属多样性降低。我们认为，由于奠基者事件，该位点的遗传多样性降低了，但尽管存在瓶颈效应，自交不亲和在旧世界仍得以维持。密码子替换模式的最大似然分析表明，旧世界的正向达尔文选择相对较强，这表明瓶颈效应后S-RNases重新多样化。因此，目前的数据除了支持米勒和维纳布尔（2000年）模型的一个关键假设，即自交不亲和与二倍体和雌雄同体相关外，还为贝克法则提供了一个显著例外。
