Widespread occurrence of asexual reproduction in higher termites of the Termes group (Termitidae: Termitinae)

Simon Hellemans,Denis Fournier,Klára Dolejšová,Jan Křivánek,Robert Hanus,Yves Roisin

doi:10.1186/s12862-019-1459-3

Abstract

BackgroundA decade ago, the mixed reproductive strategy Asexual Queen Succession (AQS) was first described in termites. In AQS species, the workers, soldiers and dispersing reproductives are produced through sexual reproduction, while non-dispersing (neotenic) queens arise through automictic thelytokous parthenogenesis, replace the founding queen and mate with the founding king. As yet, AQS has been documented in six species from three lineages of lower (Rhinotermitidae) and higher (Termitinae: Termes group and Syntermitinae) termites. Independent evolution of the capacity of thelytoky as a preadaptation to AQS is supported by different mechanisms of automixis in each of the three clades. These pioneering discoveries prompt the question on the extent of thelytoky and AQS in the diversified family of higher termites.ResultsHere, we investigated the capacity of thelytoky and occurrence of AQS in three species from the phylogenetic proximity of the neotropical AQS species Cavitermes tuberosus (Termitinae: Termes group): Palmitermes impostor, Spinitermes trispinosus, and Inquilinitermes inquilinus. We show that queens of all three species are able to lay unfertilized eggs, which undergo thelytokous parthenogenesis (via gamete duplication as in C. tuberosus) and develop through the transitional stage of aspirants into replacement neotenic queens.ConclusionsThe breeding system in P. impostor is very reminiscent of that described in C. tuberosus and can be characterized as AQS. In the remaining two species, our limited data do not allow classifying the breeding system as AQS; yet, also in these species the thelytokous production of neotenic females appears to be a systematic element of reproductive strategies. It appears likely that the capacity of thelytokous parthenogenesis evolved once in the Termes group, and may ultimately be found more widely, well beyond these Neotropical species.

Highlights

No sign of null alleles was detected at the population level for none of the species, except at loci Ctub-21 and Ctub-72 in P. impostor as suggested by the general excess of homozygotes
Our results demonstrate that queens of three species of South American Termitinae from the Termes group (Palmitermes impostor, Spinitermes trispinosus and Inquilinitermes inquilinus) are able to lay unfertilized eggs, which undergo thelytokous parthenogenesis and are destined to develop into replacement neotenic queens through a series of nymphal stages and a special transitional stage of aspirants [17]
Asexual Queen Succession (AQS) in Palmitermes impostor The conditional parthenogenesis observed in P. impostor appears to be a stable element of the breeding system of this species, which complies with the definition of the mixed reproductive strategy known as asexual queen succession (AQS)

Summary

Introduction

In AQS species, the workers, soldiers and dispersing reproductives are produced through sexual reproduction, while non-dispersing (neotenic) queens arise through automictic thelytokous parthenogenesis, replace the founding queen and mate with the founding king. The queens lay unfertilized eggs that undergo automictic thelytokous parthenogenesis and are destined to develop through a series of nymphal stages into replacement neotenic queens These non-dispersing queens, present sometimes in large numbers reaching up to several hundreds, replace their mother at some moment of the colony development and mate with the founding king, making up a “harem” breeding structure typical for AQS. The combination of sexual and asexual processes maximizes the genetic input of the queen(s) into the generation of non-dispersing queens while conserving a high genetic diversity in sterile helpers (workers and soldiers) and dispersers (future kings and queens). AQS brings two main advantages at Hellemans et al BMC Evolutionary Biology (2019) 19:131 the colony level: (i) it increases the reproductive potential of the colony through the replacement of one founding female by multiple queens bearing an undiluted gene pool of the founding queen, and (ii) it extends the colony lifespan due to the ability of the replacement queens to produce subsequent generations of parthenogens developing into neotenic queens, leading to a virtual “genetic immortality” of the foundress (reviewed in [2])

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Conclusion