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. 2023 Jan 1;23(1):9.
doi: 10.1093/jisesa/ieac073.

Same-sex Pairs Retain Their Reproductive Capacity as a Potential Opportunity for Individual Reproductive Success in Termites

Jia Wu  1   2 , Jinpei Wang  1   2   3 , Yonghui Wang  4 , Ali Hassan  5
Affiliations

Same-sex Pairs Retain Their Reproductive Capacity as a Potential Opportunity for Individual Reproductive Success in Termites

Jia Wu et al. J Insect Sci. .

Abstract

In eusocial termites, successful pairing is an essential element of dispersal and distribution after the departure of alates from natal colonies. Two situations could arise during the pairing process: mixed-sex pairs and same-sex pairs. However, most previous studies focused on mixed-sex pairs, overlooking groups formed by same-sex pairings, especially potential fecundity (the total number of oocytes or ovarioles), oogenesis and the development stage of oocytes of females in female-female pairs, and spermatogenesis and testis development of males in male-male pairs. In this study, through experimentation, we investigated the reproductive ability of virgin dealates based on various pairing types as mentioned above. We found that the life spans of virgin dealates can cover 1 yr or even more when they establish a nest with a partner, which is more than 10-fold longer than the life span of individuals establishing a colony alone. After 1 yr of pairing, the potential fecundity of virgin same sex dealates did not degenerate significantly compared with newly emerged dealates, including the number of ovarioles, size of testis, oogenesis, and the development stage of the oocytes. Moreover, when individuals of same-sex pairings experimentally changed into mixed-sex pairs after 1 yr, the eggs produced in the colony hatched into larvae. These findings suggest that dealates which through same-sex pairs retain fecundity after 1 yr have more reproductive potential than dealates that failed to pair with heterosexuals, shedding light on the ecological significance of homosexual behaviors in terms of the successful extension and fecundity of eusocial termites.

Keywords: colony fusion; gonadal development; homosexuality; life span; termite.

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Figures

Graphical Abstract
Graphical Abstract
Fig. 1.
Fig. 1.
The survival rate of homosexual pairs and heterosexual pairs. Survival was no significantly different in female–female, male–male, and female–male colonies (F = 0.13, P = 0.87).
Fig. 2.
Fig. 2.
The morphological characteristics and number of ovarioles in the ND and YD. (A) the morphological characteristics of ovarioles; (B) the number of ovarioles the ND and YD (n = 20). The number of ovarioles in the ND and YD was no significant difference (Fig. 2B; t = 0.99, P = 0.32). ND, newly dealate; YD, year-old dealate.
Fig. 3.
Fig. 3.
The morphological characteristics and size of testis in ND and YD. (A) The morphological characteristics of testis; (B) the diameter of testis in ND and YD (n = 18). The diameter of testis in ND and YD was no significant difference (Fig. 3B; t = 0.47, P = 0.64). T, testis; AG, accessory gland; ND, newly dealate; YD, year-old dealate.
Fig. 4.
Fig. 4.
The oogenesis and the number of oocytes in different stage. (A) the oogenesis; (B) the number of oocytes in oocyte growth stage and oocyte vitellogenesis stage. DO, oogonium differentiation stage; GO, oocyte growth stage; VO, oocyte vitellogenesis stage.
Fig. 5.
Fig. 5.
The spermatogenesis and the number of spermatozoa in testis. (A) The spermatogenesis; (B) the number of spermatozoa in testis. St, spermatids; Sp, spermatozoa A: Egg production in different pairs; B: the number of larvae in different pair combinations. Newly dealates pairs laid more egg (F = 23.99, P < 0.001) and larvae (F = 12.58, P = 0.002) than year-old dealates pairs. ND, newly dealate; YD, year-old dealate.
Fig. 6.
Fig. 6.
(A) Egg production in different pairs; (B) the number of larvae in different pair combinations. Newly dealates pairs laid more egg (F = 23.99, P < 0.001) and larvae (F = 12.58, P = 0.002) than year-old dealates pairs. ND, newly dealate; YD, year-old dealate.
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