Evolution of the asexual queen succession system and its underlying mechanisms in termites

Matsuura, Kenji

doi:10.1242/jeb.142547

Cited by 49 publications

(64 citation statements)

References 52 publications

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“…In other Cataglyphis species groups, recently mated queens typically found new colonies via solitary dispersal, a stressful period that probably selects against low‐fitness, clonal queens ( C. tartessica is the only known species from these groups that disperses with workers; Amor et al, ). Indeed, queen parthenogenesis has never been observed in solitary founding queens in ants (Fournier et al, ; Okamoto, Kobayashi, Hasegawa, & Ohkawara, ; Pearcy et al, ; Peeters & Aron, ) or termites (Matsuura, ; Matsuura, ).…”

Section: Discussionmentioning

confidence: 99%

Repeated evolution of queen parthenogenesis and social hybridogenesis in Cataglyphis desert ants

et al. 2019

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Over the last decade, genetic studies on social insects have revealed a remarkable diversity of unusual reproductive strategies, such as male clonality, female clonality, and social hybridogenesis. In this context, Cataglyphis desert ants are useful models because of their unique reproductive systems. In several species, queens conditionally use sexual reproduction and parthenogenesis to produce sterile workers and reproductive queens, respectively. In social hybridogenesis, two distinct genetic lineages coexist within a population, and workers result from mating between partners of different lineages; in contrast, queens and males are both produced asexually by parthenogenesis. Consequently, nonreproductive workers are all interlineage hybrids, whereas reproductives are all pure lineage individuals. Here, we characterized the reproductive systems of 11 species to investigate the distribution of the conditional use of sex and social hybridogenesis in Cataglyphis. We identified one new case in which sexual reproduction was conditionally used in the absence of dependent‐lineage reproduction. We also discovered five new instances of social hybridogenesis. Based on our phylogenetic analyses, we inferred that both the conditional use of sex and social hybridogenesis independently evolved multiple times in the genus Cataglyphis.

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Section: Discussionmentioning

confidence: 99%

Repeated evolution of queen parthenogenesis and social hybridogenesis in Cataglyphis desert ants

et al. 2019

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“…) and Cavitermes tuberosus (Termitinae) (Fournier et al . ), phylogenetically remote from Reticulitermes , suggests that the actual frequency of this outstanding breeding system across the phylogenetic diversity of Isoptera may be much higher than previously estimated (Matsuura ).…”

Section: Introductionmentioning

confidence: 85%

“…She enjoys virtual ‘genetic immortality’, limited only by the lifespan of the colony as a whole (Matsuura et al . ; Matsuura , ). In long‐lived species, AQS may have additional impacts on colony genetic structure, resulting from an eventual replacement of the founding primary king upon his death by a sexually produced neotenic one, which carries genes of the primary king and queen in equal proportions.…”

Section: Introductionmentioning

confidence: 99%

“…If commonplace in the population, such a bias increases the relative reproductive value of dispersing females and favours a female‐biased disperser sex ratio (Kobayashi et al . ; Matsuura ).…”

Section: Introductionmentioning

confidence: 99%

“…However, the three AQS species belong to three phylogenetically and geographically distinct lineages within the species‐rich genus Reticulitermes , suggesting an independent evolution of AQS in the three cases (Dedeine et al . ; Matsuura ). More importantly, we recently showed that AQS also occurs in the family Termitidae (higher termites), the most diversified and abundant termite clade.…”

Section: Introductionmentioning

confidence: 99%

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Asexual queen succession mediates an accelerated colony life cycle in the termite Silvestritermes minutus

et al. 2017

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Mixed modes of reproduction, combining sexual processes with thelytokous parthenogenesis, occur in all major clades of social insects. In several species of termites, queens maximize their genetic input into nondispersing replacement queens through parthenogenesis, while maintaining genetically diverse sterile offspring and dispersing reproductives via sexual reproduction. This so-called asexual queen succession (AQS) has multiple independent origins and its presumed advantages are diverse as well, ranging from multiplication of colony reproductive potential to extension of its lifespan beyond that of the foundress. However, how AQS shapes colony life cycles under natural conditions remains poorly known. The neotropical termite Silvestritermes minutus inhabits small but conspicuous nests, offering a unique opportunity to investigate the impact of AQS on life history. We report on its breeding system, life cycle and sex allocation using social structure census in 137 nests and genotyping of 12 colonies at 12 microsatellite loci. We show that colonies are established by an outbred pair of primary reproductives. In less than 2 years, the foundress is replaced by multiple neotenic queens, arising mostly through automixis with central fusion. Sterile castes, male and most (93%) female dispersers are produced sexually. Colony reproduction is usually restricted to a single dispersal of alates with unbiased sex ratio, taking place after 3 years. We conclude that S. minutus benefits from AQS to maximize colony growth rate and alate production within a very short life cycle rather than to extend colony lifespan. This highlights the versatile role of AQS in different cases of its polyphyletic origin.

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Genomic imprinting and evolution of insect societies

Matsuura

2019

Population Ecology

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Reproductive division of labor is a hallmark of social insect societies where individuals follow different developmental pathways resulting in distinct morphological castes.There has been a long controversy over the factors determining caste fate of individuals in social insects. Increasing evidence in the last two decades for heritable influences on division of labor put an end to the assumption that social insect broods are fully totipotent and environmental factors alone determine castes. Nevertheless, the genes that underlie hereditary effects on division of labor have not been identified in any social insects. Studies investigating the hereditary effects on caste determination might have overlooked non-genetic inheritance, while transmission to offspring of factors other than DNA sequences including epigenetic states can also affect offspring phenotype. Genomic imprinting is one of the most informative paradigms for understanding the consequences of interactions between the genome and the epigenome. Recent studies of genomic imprinting show that genes can be differentially marked in egg and sperm and inheritance of these epigenetic marks cause genes to be expressed in a parental-origin-specific manner in the offspring. By reviewing both the eusocial Hymenoptera and termites, I highlight the current theoretical and empirical evidence for genomic imprinting in eusocial insects and discuss how genomic imprinting acts in caste determination and social behavior and challenges for future studies. I also introduce the new idea that genomic imprinting plays an essential role in the origin of eusociality. K E Y W O R D Scaste determination, epigenetic inheritance, eusocial insects, genomic imprinting

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Evolution of the asexual queen succession system and its underlying mechanisms in termites

Cited by 49 publications

References 52 publications

Repeated evolution of queen parthenogenesis and social hybridogenesis in Cataglyphis desert ants

Repeated evolution of queen parthenogenesis and social hybridogenesis in Cataglyphis desert ants

Asexual queen succession mediates an accelerated colony life cycle in the termite Silvestritermes minutus

Genomic imprinting and evolution of insect societies

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