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, 111 (48), 17212-7

Termite Queens Close the Sperm Gates of Eggs to Switch From Sexual to Asexual Reproduction

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Termite Queens Close the Sperm Gates of Eggs to Switch From Sexual to Asexual Reproduction

Toshihisa Yashiro et al. Proc Natl Acad Sci U S A.

Abstract

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.

Keywords: Isoptera; asexual queen succession; egg fertilization; micropyle; thelytoky.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Colony development and asexual queen succession in the termite R. speratus. As the primary queen senesces, secondary queens produced asexually by the primary queen differentiate within the colony and supplement egg production, eventually replacing the primary queen (details described in SI Text). Squares indicate males, and circles represent females. PK, primary king; PQ, primary queen; SQ, secondary queen. (Scale bars: 3 mm.)
Fig. 2.
Fig. 2.
Variation in the number of micropyles of eggs. (A) Scanning electron microscope image of the posterior end of an egg with micropyles (ventral view). (Scale bar: 50 μm.) (B) Confocal scanning laser microscope image of micropyles (close-up view). (Scale bar: 10 μm.) (C) Posterior views (dorsal up) of representative eggs with different numbers of micropyles (zero, two, four, and nine). Micropyles were visualized by eosin Y staining. (Scale bar: 100 μm.) (D) Comparison of the number of micropyles among 4 representative colonies (n = 100 for each colony) and the total of 60 field colonies (n = 6,000). Micropyleless eggs are indicated by red bars. MP, micropyle.
Fig. 3.
Fig. 3.
Regulation of the production of micropyleless eggs by the queens. (A) Comparisons of (Top) the size of newly differentiated secondary queens and old physogastric secondary queens in colonies (Left) YO120508A and (Right) AO140511A and frequency distributions of the numbers of micropyles of the eggs laid by (Middle) young and (Bottom) old queens. Micropyleless eggs are indicated by red bars. Blue lines show the fitted normal distributions. (B) Comparison of the proportion of the colonies with (black bars) and without (white bars) micropyleless eggs among the colonies collected in the spring (n = 9), summer (n = 35), and autumn (n = 16). Different letters on the bars indicate significant differences (P < 0.01; Fisher’s exact probability test with sequential Bonferroni correction). (C) Expectation of the proportion of micropyleless eggs based on the median and the variance of the distribution of the number of micropyles. SQ, secondary queen.

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