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The dominance of sexual reproduction is still an unresolved enigma in evolutionary biology. Strong advantages of sex have to exist, because only a few parthenogenetic taxa persist over evolutionary timescales. Oribatid mites (Acari) include outstanding exceptions to the rule that parthenogenetically reproducing taxa are of recent origin and doomed to extinction. In addition to the existence of large parthenogenetic clusters in oribatid mites, phylogenetic analyses of this study and model-based reconstruction of ancestral states of reproduction imply that Crotoniidae have reevolved sexuality from parthenogenetic ancestors within one of those clusters. This reversal in reproductive mode is unique in the animal kingdom and violates Dollo's law that complex ancestral states can never be reacquired. The reevolution of sexuality requires that ancestral genes for male production are maintained over evolutionary time. This maintenance likely is true for oribatid mites because spanandric males exist in various species, although mechanisms that enable the storage of genetically ancestral traits are unclear. Our findings present oribatid mites as a unique model system to explore the evolutionary significance of parthenogenetic and sexual reproduction.

The ecological and evolutionary opportunities of apomixis in the short and the long term are considered, based on two closely related apomictic genera: Taraxacum (dandelion) and Chondrilla (skeleton weed). In both genera apomicts have a wider geographical distribution than sexuals, illustrating the short-term ecological success of apomixis. Allozymes and DNA markers indicate that apomictic populations are highly polyclonal. In Taraxacum, clonal diversity can be generated by rare hybridization between sexuals and apomicts, the latter acting as pollen donors. Less extensive clonal diversity is generated by mutations within clonal lineages. Clonal diversity may be maintained by frequency-dependent selection, caused by biological interactions (e.g. competitors and pathogens). Some clones are geographically widespread and probably represent phenotypically plastic 'general-purpose genotypes'. The long-term evolutionary success of apomictic clones may be limited by lack of adaptive potential and the accumulation of deleterious mutations. Although apomictic clones may be considered as 'evolutionary dead ends', the genes controlling apomixis can escape from degeneration and extinction via pollen in crosses between sexuals and apomicts. In this way, apomixis genes are transferred to a new genetic background, potentially adaptive and cleansed from linked deleterious mutations. Consequently, apomixis genes can be much older than the clones they are currently contained in. The close phylogenetic relationship between Taraxacum and Chondrilla and the similarity of their apomixis mechanisms suggest that apomixis in these two genera could be of common ancestry.

Arbuscular mycorrhizal fungi (AMF) are important plant symbionts that have long been considered evolutionary anomalies because of their apparent long-term lack of sexuality, but recent explorations of available DNA sequence have challenged this notion by revealing the presence of homologues of fungal mating type-high-mobility group (MATA-HMG) and core meiotic genes in these organisms. To obtain more insights into the sexual potential of AMF, homologues of MATA-HMGs were sought in the transcriptome of three AMF isolates, and their functional and evolutionary trajectories were studied in genetically divergent strains of Rhizophagus irregularis using conventional and quantitative PCR procedures. Our analyses revealed the presence of at least 76 homologues of MATA-HMGs in R.irregularis isolates. None of these was found to be surrounded by genes generally found near other known fungal mating type loci, but here we report the presence of a 9-kb-long region in the AMF R.irregularis harbouring a total of four tandem-repeated MATA-HMGs; a feature that highlights a potentially elevated intragenomic diversity in this AMF species. The present study provides intriguing insights into the genome evolution of R.irregularis, and represents a stepping stone for understanding the potential of these fungi to undergo cryptic sex.

Ecological theories of sexual reproduction assume that sexuality is advantageous in certain conditions, for example, in biotically or abiotically more heterogeneous environments. Such theories thus could be tested by comparative studies. However, the published results of these studies are rather unconvincing. Here, we present the results of a new comparative study based exclusively on the ancient asexual clades. The association with biotically or abiotically homogeneous environments in these asexual clades was compared with the same association in their sister, or closely related, sexual clades. Using the conservative definition of ancient asexuals (i.e., age >1 million years), we found eight pairs of taxa of sexual and asexual species, six differing in the heterogeneity of their inhabited environment on the basis of available data. The difference between the environmental type associated with the sexual and asexual species was then compared in an exact binomial test. The results showed that the majority of ancient asexual clades tend to be associated with biotically, abiotically, or both biotically and abiotically more homogeneous environments than their sexual controls. In the exploratory part of the study, we found that the ancient asexuals often have durable resting stages, enabling life in subjectively homogeneous environments, live in the absence of intense biotic interactions, and are very often sedentary, inhabiting benthos, and soil. The consequences of these findings for the ecological theories of sexual reproduction are discussed. Ecological theories of sexual reproduction assume that sexuality is advantageous in certain conditions, for example, in biotically or abiotically more heterogeneous environments. Using available literature, we identified six groups of long‐term asexual eukaryotes for which relevant ecological data are available and found their environment to be significantly more often biotically and abiotically more homogeneous than the environment of their sexual relatives. Particular aspects of ancient asexuals’ environments, as well as the theoretical implications of our findings, are discussed.

Ostracods are one of the oldest crustacean groups with an excellent fossil record and high importance for phylogenetic analyses but genome resources for this class are still lacking. We have successfully assembled and annotated the first reference genomes for three species of nonmarine ostracods; two with obligate sexual reproduction (Cyprideis torosa and Notodromas monacha) and the putative ancient asexual Darwinula stevensoni. This kind of genomic research has so far been impeded by the small size of most ostracods and the absence of genetic resources such as linkage maps or BAC libraries that were available for other crustaceans. For genome assembly, we used an Illumina-based sequencing technology, resulting in assemblies of similar sizes for the three species (335–382 Mb) and with scaffold numbers and their N50 (19–56 kb) in the same orders of magnitude. Gene annotations were guided by transcriptome data from each species. The three assemblies are relatively complete with BUSCO scores of 92–96. The number of predicted genes (13,771–17,776) is in the same range as Branchiopoda genomes but lower than in most malacostracan genomes. These three reference genomes from nonmarine ostracods provide the urgently needed basis to further develop ostracods as models for evolutionary and ecological research.

Phylogenetic and phylogeographic studies suggest that a majority of asexual organisms are evolutionarily recent offshoots of extant sexual taxa and that old clonal lineages tend to be isolated from their sexual and younger asexual counterparts. These observations have often been interpreted as support for the long-term disadvantages of asexuality resulting from the mechanisms of clonal decay. Although clonal decay is likely to be an important mechanism that limits the temporal and spatial distribution of asexual lineages, we argue here that contemporary phylogenetic analyses, which are mostly restricted to simple comparisons of “recent” and “ancient” clones, need to be tested against an appropriate null model of neutrality. We use computer simulations to show that many empirical observations of the distribution of asexuality do not in fact reject a null model of the neutral turnover of clones spawned by sexual relatives. In particular, neutral clonal turnover results in qualitatively similar pattern of clonal spatial distribution and age structure, as does a process that includes clonal decay. Although there are important quantitative differences between predictions made by the two models, we show that published empirical data are still inadequate to distinguish between them. Further work on sexual-asexual complexes is therefore required before clonal turnover can be rejected as a parsimonious explanation of the spatial distribution and age structure of asexual lineages.

Many unisexual animal lineages supposedly arose from hybridization. However, support for their putative hybrid origins mostly comes from indirect methodologies, which are rarely confirmatory. Here we provide compelling data indicating that tetraploid unisexual Calligrapha are true genetic mosaics obtained via analysis of mitochondrial DNA (mtDNA) and allelic variation and coalescence times for three single-copy nuclear genes (CPS, HARS, and Wg) in five of six unisexual Calligrapha and a representative sample of bisexual species. Nuclear allelic diversity in unisexuals consistently segregates in the gene pools of at least two but up to three divergent bisexual species, interpreted as putative parentals of interspecific hybridization crosses. Interestingly, their mtDNA diversity derives from an additional yet undiscovered older evolutionary lineage that is possibly the same for all independently originated unisexual species. One possibly extinct species transferred its mtDNA to several evolutionary lineages in a wave of hybridization events during the Pliocene, whereby descendant species retained a polymorphic mtDNA constitution. Recent hybridizations, in the Pleistocene and always involving females with the old introgressed mtDNA, seemingly occurred in the lineages leading to unisexual species, decoupling mtDNA introgression (and inferences derived from these data, such as timing and parentage) from subsequent acquisition of the new reproductive mode. These results illuminate an unexpected complexity in possible routes to animal unisexuality, with implications for the interpretation of ancient unisexuality. If the origin of unisexuality requires a mechanism where (1) hybridization is a necessary but insufficient condition and (2) multiple bouts of hybridization involving more than two divergent lineages are required, then the origins of several classical unisexual systems may have to be reassessed.

Fully asexual lineages cannot purge accumulating mutations from their genome through recombination. In ancient asexuals that have persisted without sex for millions of years, this should lead to high allelic divergences (the 'Meselson effect') as has been shown for bdelloid rotifers. Homogenizing mechanisms can counter this effect, resulting in low genetic diversity within and between individuals. Here, we show that the ancient asexual ostracod species Darwinula stevensoni has very low nucleotide sequence divergence in three nuclear regions. Differences in genetic diversity between embryos and adults furthermore indicate that up to half of the observed genetic changes in adults can be caused by somatic mutations. Likelihood permutation tests confirm the presence of gene conversion in the multi-copy internal transcribed spacer sequence, but reject rare or cryptic forms of sex as a general explanation for the low genetic diversity in D. stevensoni. Other special mechanisms (such as highly efficient DNA repair) might have been selected for in this ancient asexual to overcome the mutational load and Muller's ratchet. In this case, our data support these hypotheses on the prevalence of sex, even if the two extant ancient asexual groups (bdelloids and darwinulids) seem to follow opposite evolutionary strategies.

Arbuscular mycorrhizal fungi (AMF) form extremely important mutualistic symbioses with most plants. Their role in nutrient acquisition, plant community structure, plant diversity, and ecosystem productivity and function has been demonstrated in recent years. New findings on the genetics and biology of AMF also give us a new picture of how these fungi exist in ecosystems. In this article, I bring together some recent findings that indicate that AMF have evolved to contain multiple genomes, that they connect plants together by a hyphal network, and that these different genomes may potentially move around in this network. These findings show the need for more intensive studies on AMF population biology and genetics in order to understand how they have evolved with plants, to better understand their ecological role, and for applying AMF in environmental management programs and in agriculture. A number of key features of AMF population biology have been identified for future studies and most of these concern the need to understand drift, selection, and genetic exchange in multigenomic organisms, a task that has not previously presented itself to evolutionary biologists.