Queen Succession Through Asexual Reproduction in Termites

Matsuura, Kenji; Vargo, Edward L.; Kawatsu, Kazutaka; Labadie, Paul; Nakano, Hiroko; Yashiro, Toshihisa; Tsuji, Kazuki

doi:10.1126/science.1169702

Cited by 151 publications

(204 citation statements)

References 7 publications

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“…On the other hand, primary kings live much longer than primary queens. This AQS system enables founding queens to increase their reproductive output while retaining the same transmission rate of their genes to future generations 19,20,23 (Fig. 3b).…”

Section: Resultsmentioning

confidence: 99%

“…Recently, a novel breeding system called AQS has been described in two species of subterranean termites-Reticulitermes speratus 19 and Reticulitermes virginicus 20 -that meet all three of these conditions. Termite colonies are typically founded by a monogamous pair of primary reproductives (adult winged forms), one king and one queen.…”

Section: Resultsmentioning

confidence: 99%

“…In the subterranean termites R. speratus and R. virginicus, queens produce their neotenic replacement reproductives asexually but use normal sexual reproduction to produce other colony members 19,20 . These species undergo typical colony founding by a pair of primary reproductives.…”

Section: Resultsmentioning

confidence: 99%

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Sex ratio biases in termites provide evidence for kin selection

et al. 2013

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Inclusive fitness theory, also known as kin selection theory, is the most general expansion of Darwin's natural selection theory. It is supported by female-biased investment by workers in the social Hymenoptera where relatedness to sisters is higher than to brothers because of haplodiploidy. However, a strong test of the theory has proven difficult in diploid social insects because they lack such relatedness asymmetry. Here we show that kin selection can result in sex ratio bias in eusocial diploids. Our model predicts that allocation will be biased towards the sex that contributes more of its genes to the next generation when sex-asymmetric inbreeding occurs. The prediction matches well with the empirical sex allocation of Reticulitermes termites where the colony king can be replaced by a queen's son. Our findings open broad new avenues to test inclusive fitness theory beyond the well-studied eusocial Hymenoptera.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Sex ratio biases in termites provide evidence for kin selection

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“…Conversely, overproduction of parthenogenetic offspring would impose a large cost on colonies, because these individuals are inferior to sexually produced individuals as workers or alates, likely because of their complete loss of heterozygosity (14,28). Therefore, selection should act against overproduction of parthenogenetic eggs and favor the production of necessary minimum numbers of micropyleless eggs.…”

Section: Resultsmentioning

confidence: 99%

“…S1) (18,19). In AQS species, queens produce their neotenic replacement queens asexually but use normal sexual reproduction to produce other colony members (14)(15)(16). Because sex determination in Reticulitermes termites is male heterogamy (20), queens cannot produce secondary kings by parthenogenesis (17).…”

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Termite queens close the sperm gates of eggs to switch from sexual to asexual reproduction

Yashiro

Matsuura

2014

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

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Males and females are in conflict over genetic transmission in the evolution of parthenogenesis, because it enhances female reproductive output but deprives the males' genetic contribution. For males, any trait that coerces females into sexual reproduction should increase their fitness. However, in the termite Reticulitermes speratus, queens produce their replacements (neotenic queens) parthenogenetically while using normal sexual reproduction to produce other colony members. Here, we show that termite queens produce parthenogenetic offspring in the presence of kings by closing the micropyles (sperm gates; i.e., openings for sperm entry) of their eggs. Our field survey showed that termite eggs show large variation in numbers of micropyles, with some having none. Microsatellite analysis showed that embryos of micropyleless eggs develop parthenogenetically, whereas those of eggs with micropyles are fertilized and develop sexually. Surveys of eggs among queens of different age groups showed that queens begin to lay micropyleless eggs when they are older and thus, need to produce their replacements parthenogenetically. In addition, we found clear seasonality in new neotenic queen differentiation and micropyleless egg production. This micropyle-dependent parthenogenesis is the first identification, to our knowledge, of the mechanism through which females control egg fertilization over time in diploid animals, implying a novel route of the evolution of parthenogenesis in favor of female interests without interference from males.thelytoky | micropyle | asexual queen succession | egg fertilization | Isoptera

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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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Queen Succession Through Asexual Reproduction in Termites

Cited by 151 publications

References 7 publications

Sex ratio biases in termites provide evidence for kin selection

Sex ratio biases in termites provide evidence for kin selection

Termite queens close the sperm gates of eggs to switch from sexual to asexual reproduction

Genomic imprinting and evolution of insect societies

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