Mol Ecol. 2021 Dec;30(24):6743-6758. doi: 10.1111/mec.16185. Epub 2021 Oct 04.

Extra-pair paternity in the wood-feeding cockroach Cryptocercus punctulatus Scudder: Social but not genetic monogamy.

Molecular ecology

Hajime Yaguchi, Itaru Kobayashi, Kiyoto Maekawa, Christine A Nalepa

PMID: 34543485 DOI: 10.1111/mec.16185

Abstract

Subsocial Cryptocercus cockroaches are the sister group to termites and considered to be socially monogamous. Because genetic monogamy is a suggested requirement for evolution of cooperative breeding/eusociality, particularly in hymenopterans, clarification of the mating biology of Cryptocercus would help illuminate evolutionary trends in eusocial insects. To investigate possible extra-pair paternity in C. punctulatus, microsatellite markers were used to analyse offspring parentage, the stored sperm in females and results of experimental manipulation of sperm competition. Extra-pair paternity was common in field-collected families, but a lack of maternal alleles in several nymphs suggests sampling error or adoption. Isolating prereproductive pairs and assaying subsequently produced nymphs confirmed that nymphs lacked alleles from the pair male in 40% of families, with extra-pair male(s) siring 27%-77% of nymphs. Sperm of extra-pair males was detected in the spermatheca of 51% of paired prereproductive females. Mate switching and surgical manipulation of male mating ability indicated a tendency towards last male sperm precedence. Overall, the results demonstrate that about half of young females are serially monogamous during their maturational year, but bond, overwinter and produce their only set of offspring in company of the last mated male (=pair male). Repeated mating by the pair male increases the number of nymphs sired, but because many females use stored sperm of previous copulatory partners to fertilize eggs, pair males extend parental care to unrelated nymphs. The results suggest that genetic monogamy either developed in the termite ancestor after splitting from the Cryptocercus lineage, or that genetic monogamy may not be a strict prerequisite for the evolution of termite eusociality.

© 2021 John Wiley & Sons Ltd.

Keywords: eusociality; paternity; semelparity; serial monogamy; subsociality; termite

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