A Case of Reversal: The Evolution and Maintenance of Sexuals from Parthenogenetic Clones in<i>Hieracium pilosella</i>

Chapman, Hazel M.; Houliston, Gary J.; Robson, Beth; Iline, I.I.

doi:10.1086/376819

Cited by 49 publications

(39 citation statements)

References 37 publications

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“…Although evolutionary reversals from less complex to more complex ancestral traits have long been deemed unlikely (46,47), reversals from asexual to sexual reproduction have been suggested for mites and hawkweed (48,49). The absence of males (17) and the lack of genetic recombination in asexual populations of M. smithii are consistent with the hypothesis that meiosis is dysfunctional in parthenogenetic queens.…”

Section: Resultssupporting

confidence: 66%

Cryptic sexual populations account for genetic diversity and ecological success in a widely distributed, asexual fungus-growing ant

Rabeling

Gonzales

Schultz

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Sex and recombination are central processes in life generating genetic diversity. Organisms that rely on asexual propagation risk extinction due to the loss of genetic diversity and the inability to adapt to changing environmental conditions. The fungus-growing ant species Mycocepurus smithii was thought to be obligately asexual because only parthenogenetic populations have been collected from widely separated geographic localities. Nonetheless, M. smithii is ecologically successful, with the most extensive distribution and the highest population densities of any fungus-growing ant. Here we report that M. smithii actually consists of a mosaic of asexual and sexual populations that are nonrandomly distributed geographically. The sexual populations cluster along the Rio Amazonas and the Rio Negro and appear to be the source of independently evolved and widely distributed asexual lineages, or clones. Either apomixis or automixis with central fusion and low recombination rates is inferred to be the cytogenetic mechanism underlying parthenogenesis in M. smithii. Males appear to be entirely absent from asexual populations, but their existence in sexual populations is indicated by the presence of sperm in the reproductive tracts of queens. A phylogenetic analysis of the genus suggests that M. smithii is monophyletic, rendering a hybrid origin of asexuality unlikely. Instead, a mitochondrial phylogeny of sexual and asexual populations suggests multiple independent origins of asexual reproduction, and a divergence-dating analysis indicates that M. smithii evolved 0.5-1.65 million years ago. Understanding the evolutionary origin and maintenance of asexual reproduction in this species contributes to a general understanding of the adaptive significance of sex.Attini | clonality | Formicidae | thelytoky | mutualism T he vast majority of metazoans reproduces sexually, enjoying the benefits of genetic recombination (1-3) such as rapid adaptability to novel ecological conditions (4, 5) and the purging of deleterious mutations from their genomes (6, 7). However, relative to sexually reproducing organisms, an asexual female doubles its fitness by transmitting its entire genetic material to the next generation (8). Despite such obvious short-term fitness advantages, asexual organisms occur only sporadically throughout the tree of life and are predicted to be evolutionarily short-lived and doomed to early extinction (9-11). In contrast to the short-term advantages of asexuality, the adaptive value of sexuality, that is, genetic recombination, is expected to be of long-term benefit (2, 12-14). There remain in evolutionary biology significant unexplored questions about whether sexual reproduction is favored by natural selection over short evolutionary time spans and, if not, why sexual reproduction persists as the prevalent mode of reproduction, given that the selective benefits are deferred. Studying the origin and evolution of parthenogenetic lineages, and understanding how genetic diversity is generated and preserved in such linea...

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Section: Resultssupporting

confidence: 66%

Cryptic sexual populations account for genetic diversity and ecological success in a widely distributed, asexual fungus-growing ant

Rabeling

Gonzales

Schultz

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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“…Atavisms are also present in humans (28). Another example relates to reproductive biology; the plant Hieracium pilosella (29) reevolved sexuality but from a recent and narrow parthenogenetic lineage. The reevolution of sexuality in ancient parthenogenetic clusters of oribatid mites as suggested by this study is, to our knowledge, previously unrecognized in the animal kingdom.…”

Section: Discussionmentioning

confidence: 99%

Reevolution of sexuality breaks Dollo's law

Domes

Norton

Maraun

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

138

115

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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.oribatid mites ͉ parthenogenesis ͉ spanandric males ͉ automixis ͉ ancient asexuals

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“…Apomixis has previously been considered as an evolutionary dead end, as it is associated with loss of the ability to generate genetic variation through recombination, which renders apomictic populations incapable of adapting to environmental change. However, the incomplete penetrance of apomixis and maintenance of a normal sexual pathway in most apomicts provides opportunity for genetic diversification and evolution via sexual recombination (Chapman et al 2003;Hörandl and Hojsgaard 2012).…”

Section: Genetics and Inheritance Of Apomixismentioning

confidence: 99%

The Genetic Control of Apomixis: Asexual Seed Formation

2014

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Apomixis (asexual seed formation) is the result of a plant gaining the ability to bypass the most fundamental aspects of sexual reproduction: meiosis and fertilization. Without the need for male fertilization, the resulting seed germinates a plant that develops as a maternal clone. This dramatic shift in reproductive process has been documented in many flowering plant species, although no major seed crops have been shown to be capable of apomixis. The ability to generate maternal clones and therefore rapidly fix desirable genotypes in crop species could accelerate agricultural breeding strategies. The potential of apomixis as a nextgeneration breeding technology has contributed to increasing interest in the mechanisms controlling apomixis. In this review, we discuss the progress made toward understanding the genetic and molecular control of apomixis. Research is currently focused on two fronts. One aims to identify and characterize genes causing apomixis in apomictic species that have been developed as model species. The other aims to engineer or switch the sexual seed formation pathway in non-apomictic species, to one that mimics apomixis. Here we describe the major apomictic mechanisms and update knowledge concerning the loci that control them, in addition to presenting candidate genes that may be used as tools for switching the sexual pathway to an apomictic mode of reproduction in crops.

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A Case of Reversal: The Evolution and Maintenance of Sexuals from Parthenogenetic Clones inHieracium pilosella

Cited by 49 publications

References 37 publications

Cryptic sexual populations account for genetic diversity and ecological success in a widely distributed, asexual fungus-growing ant

Cryptic sexual populations account for genetic diversity and ecological success in a widely distributed, asexual fungus-growing ant

Reevolution of sexuality breaks Dollo's law

The Genetic Control of Apomixis: Asexual Seed Formation

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