Gómez-Zurita Jesús, Funk Daniel J, Vogler Alfried P
Department of Entomology, The Natural History Museum, London, United Kingdom.
Evolution. 2006 Feb;60(2):328-47.
Interspecific hybridization is a well-established cause of unisexual origins in vertebrates. This mechanism is also suspected in other apomictic taxa, but compelling evidence is rare. Here, we evaluate this mechanism and other hypotheses for the evolutionary origins of unisexuality through an investigation of Calligrapha leaf beetles. This group provides an intriguing subject for studies of unisexual evolution because it presents a rare insect example of multiple apomictic thelytokous species within a primarily bisexual genus. To investigate unisexual evolution, this study conducts the first molecular systematic analysis of Calligrapha. This involved the collection and analysis of about 3000 bp of DNA sequences--representing RNA and protein-coding loci from mitochondrial and nuclear genomes--from 54 specimens of 25 Calligrapha species, including four unisexual tetraploid taxa. Phylogenetic and molecular clock analyses indicated independent and single evolutionary origins of each of these unisexual species during the Pleistocene. Significant phylogenetic incongruence was detected between mitochondrial and nuclear datasets and found to be especially associated with the asexual taxa. This pattern is expected when unisexual lineages arise via interspecific hybridization and thus represent genetic mosaics that possess certain nuclear alleles from the paternal species lineage and mitochondrial DNA (mtDNA) alleles from the maternal parent. Analyzing the mtDNA and nuclear relatedness of unisexuals with corresponding haplotypes of bisexual Calligrapha species allowed the putative identification of these maternal and paternal species lineages for each unisexual species. Strong phenotypic similarities between unisexual taxa and their paternal parent species supported a model that involves both backcrosses of interspecific hybrids with a paternal parent and unreduced gametes. This model accounts for the origins of apomixis, polyploidy, and an overrepresentation of paternal nuclear alleles (and associated phenotypes) in unisexuals. This model is also consistent with the tetraploid karyotypes of unisexual Calligrapha, in which three sets of chromosomes (of presumed paternal ancestry) are quite morphologically homogeneous compared to the fourth. Especially intriguing was a consistent association of unisexual species with the host plant of the paternal parent but never with the maternal host. The statistical implausibility of these patterns occurring by chance further supports our inference of parental species. Moreover, it points to a potentially critical role for host-association in the formation and preservation of unisexual lineages. These findings suggest that ecological factors are critical for the diversification of unisexual as well as bisexual taxa and thus point out new research directions in the area of ecological speciation.
种间杂交是脊椎动物单性起源的一个公认原因。在其他无融合生殖类群中也怀疑存在这种机制，但确凿的证据很少。在这里，我们通过对Calligrapha叶甲虫的调查来评估这种机制以及关于单性起源的其他假说。该类群为单性进化研究提供了一个有趣的对象，因为它呈现了一个罕见的昆虫例子，即在一个主要为两性生殖的属内有多个无融合生殖的产雌孤雌生殖物种。为了研究单性进化，本研究对Calligrapha进行了首次分子系统分析。这涉及从25种Calligrapha的54个标本中收集和分析约3000 bp的DNA序列——代表线粒体和核基因组中的RNA和蛋白质编码位点，其中包括四个单性四倍体类群。系统发育和分子钟分析表明，这些单性物种中的每一个在更新世期间都有独立且单一的进化起源。在线粒体和核数据集之间检测到显著的系统发育不一致，并且发现这与无性类群特别相关。当单性谱系通过种间杂交产生，从而代表具有来自父本物种谱系的某些核等位基因和来自母本的线粒体DNA（mtDNA）等位基因的遗传镶嵌体时，就会出现这种模式。通过分析单性个体与两性Calligrapha物种相应单倍型的mtDNA和核相关性，能够推测出每个单性物种的母本和父本物种谱系。单性类群与其父本物种之间强烈的表型相似性支持了一个模型，该模型涉及种间杂种与父本的回交以及未减数配子。这个模型解释了无融合生殖、多倍体的起源以及单性个体中父本核等位基因（和相关表型）的过度存在。这个模型也与单性Calligrapha的四倍体核型一致，其中三组染色体（假定为父本祖先）在形态上与第四组相比相当均匀。特别有趣且一致的是，单性物种与父本的寄主植物相关联，但从不与母本寄主相关联。这些模式偶然出现的统计学上的不合理性进一步支持了我们对亲本物种的推断。此外，它指出了寄主关联在单性谱系的形成和维持中可能起的关键作用。这些发现表明，生态因素对于单性以及两性类群的多样化至关重要，因此指出了生态物种形成领域的新研究方向。
