The classification of asexual organisms: Old myths, new facts, and a novel pluralistic approach

Abstract

Organisms reproducing via asexuality harbor a great diversity of lineages, morphotypes and ecotypes. However, classification of asexual taxa does not fit into contemporary species concepts, and hence the diversity of apomictic plant complexes is not well reflected in taxonomy. Plants reproducing via apomixis (i.e., asexual seed formation = agamospermy) exemplify the theoretical and practical problems of classification. Obligately asexual organisms do not form reproductive communities, but they do constitute ancestor-descendant lineages. From the conceptual side, evolutionary lineage concepts would fit best for species delimitation. Recent research showed that these lineages are not necessarily threatened by rapid extinction and do have persistence in time and space. Facultative sexuality and low levels of residual recombination counteract the accumulation of deleterious mutations due to the lack of recombination (Muller's ratchet). Apomictic lineages do have adaptive potential, which is demonstrated by the ability to occupy large distribution areas and to experience ecological niche shifts. The challenge for classification of asexual lineages, however, is to find operational criteria for species delimitation. Current practices of species delimitation can be grouped into four main principles: (1) the sexuals-first principle means that obligate sexual progenitor species are classified separately from their apomictic derivatives.(2) The all-in-one principle merges sexual progenitors and highly facultative apomictic derivatives into one species, whereby the apomicts often represent autopolyploids without differentiated phenotypes. (3) The cluster concept applies to allopolyploid complexes with facultative apomixis and a huge diversity of genotypes and morphotypes; here the main genetic clusters are treated as species. (4) Almost obligate apomictic lineages are being classified as agamospecies. The four principles reflect quite well evolutionary traits and diversity of lineages. Finally, a recommendation for a workflow is given, following this gradient from obligate sexuality to obligate apomixis.

Phylogenomics supported by geometric morphometrics reveals delimitation of sexual species within the polyploid apomicticRanunculus auricomuscomplex (Ranunculaceae)

“…Here, we present the first comprehensive phylogenomic and geometric morphometric analysis of all hitherto known sexual species of the Eurasian R. auricomus complex. The delimitation of sexual species and reconstruction of a phylogenetic framework of progenitors is an important step for the classification of apomictic polyploid complexes (Grant, 1981; Burgess & al., 2015; Hörandl, 2018). We ascertained previously reported ploidy levels and sexual mode of reproduction for all taxa by using flow cytometric methods.…”

“…In general, results of the present study raised the need for a re-classification of the described sexual species within the R. auricomus complex. On the one hand, an evolutionary ancestor-descendant lineage concept, including evolutionary role and circumscription of lineages, should be preferred for species delimitation from the conceptual point of view (De Queiroz, 2007; Freudenstein & al., 2017; Sukumaran & Knowles, 2017; Hörandl, 2018). On the other hand, the genetic cluster concept, where a species is defined as a ‘morphologically or genetically distinguishable group of individuals that has few or no intermediates when in contact with other such clusters’ (Mallet, 1995), is also well-applicable when considering the present distance-based genetic and morphometric analyses.…”

“…The basic workflow of this study: As proposed by (Hörandl, 2018) for polyploid apomictic species complexes, we first analyzed the sexual species of R. auricomus . We carried out a dual-approach based on phylogenomic data supported by geometric morphometrics to propose a well-defined species concept.…”

“…Nevertheless, its rather challenging to define their evolutionary role and circumscription, i.e. persistence in time and space, ecological niche or a shared phenotype (Freudenstein & al., 2017; Hörandl, 2018). Hörandl (2018) proposed a species delimitation workflow based on four main principles particularly addressing apomictic polyploid complexes: First, separate and classify the obligate sexual progenitor species; second, merge sexual progenitors and highly facultative apomictic lineages into one species; third, classify the main clusters of the remaining facultative apomicts as species; and fourth, treat obligate apomictic lineages as agamospecies.…”

Sex and Rosaceae apomicts

“…Moreover, pollination may still be required if successful seed-set depends on endosperm fertilization (pseudogamy; cf. box 1 in Hörandl, 2018). The modifications of gamete development and gamete fate just described are themselves subject to variation.…”