Mendelian segregation of leaf phenotypes in experimental F2hybrids elucidates origin of morphological diversity of the apomicticRanunculus auricomuscomplex

Abstract

AbstractApomictic plant complexes exhibit a stunning morphological diversity. TheRanunculus auricomuscomplex with more than 800 morphologically recognized asexual species and just 4 known sexual species is a model group to study origins of high morphological diversity in asexually reproducing lineages. During the Pleistocene, the sexuals of theR. auricomuscomplex diverged in Central Europe into two morphological groups of contrasting basal leaf phenotypes, the undivided forms represented by diploidR. carpaticolaand the deeply divided forms represented by diploidR. notabilis. An experimental interspecific crossing ofR. carpaticola×R. notabilisrevealed an extensive phenotypic diversity of the sexually formed F2hybrid generation. We hypothesize that apomictic species of the EuropeanR. auricomuscomplex might have established from hybrid derivatives ofcarpaticola‐andnotabilis‐like sexual ancestors. Here we investigate segregation of F2basal leaf phenotypes from experimentalR. carpaticola×R. notabiliscrosses. We tested the hypothesis whether F2hybrid leaf phenotypes segregate in a Mendelian manner and whether any segregant phenotypes matchR. variabilis, an apomictic species and natural hybrid derivative ofR. notabilis. Using landmark‐based geometric morphometrics of basal leaves, we recognized two major morphological clusters within theR. carpaticola×R. notabilisF2hybrid population. Thecarpaticola‐like morphological cluster included undivided or less‐divided leaf phenotypes without lateral sinuses and thenotabilis‐like morphological cluster contained deeply divided leaf phenotypes with 1–2 lateral sinuses. The overall ratio of the both morphological clusters within the F2hybrid population was approximately 1 : 1, suggesting Mendelian inheritance and partial dominance of the allele for the divided leaf phenotype. The morphological cluster of divided leaf phenotypes included 11% of F2individuals with a higher similarity to the apomictic speciesR. variabilisthan to the parental sexuals. Thevariabilis‐like F2segregant phenotypes often resulted from F1 crosses ofcarpaticola‐like mother plants withnotabilis‐like pollen donors; such crossing lines reached the highest morphological disparity. Equivalent hybridizations in nature followed by Mendelian segregation of phenotypes, which became later on fixed via the shift to apomictic reproduction, might have established the extant diversity of apomictic complexes. Microsatellite genotyping with six SSR loci revealed no correlation of genetic and phenotypic variation. We conclude that former “morpho‐groups” or “main species” based on phenotypic similarity only are unsuitable units for taxonomic classification.