Asexual queen succession in termites (A29115)
1 Title: Asexual queen succession in termites
2
3 eLS ID: A29115
4 DOI: 10.1002/9780470015902.a0029115
5
6 Author names and Affiliations
7 Simon Hellemans1,2,*, Yves Roisin2
8 1Okinawa Institute of Science & Technology Graduate University, 1919-1 Tancha, Onna-son,
9 Okinawa 904-0495, Japan.
10 2Evolutionary Biology & Ecology, Université Libre de Bruxelles, Avenue F.D. Roosevelt 50,
11 CP 160/12, B-1050 Brussels, Belgium.
1 Asexual queen succession in termites (A29115)
12 Article level: Advanced
13
14 Abstract
15 Termite species from phylogenetically distant lineages were shown to combine both sexual and
16 parthenogenetic reproductions, in a breeding system dubbed as “Asexual Queen Succession”.
17 Queens of these species use sexual reproduction for the production of the workforce and
18 dispersers, and thelytokous parthenogenesis for the production of non-dispersing queens. These
19 new queens, often produced in large numbers, will replace their mother upon her death and
20 mate with the founding king. Replacement by these parthenogens maintains the colony’s
21 genetic diversity and enhances its growth rate, lifespan and reproductive potential. This
22 breeding system also allows the efficient purging of recessive deleterious mutations from the
23 genomes, and contributes to shape the population sex ratio of these species. This conditional
24 parthenogenesis evolved from a diverse cytological background, and in phylogenetically distant
25 species with contrasted lifestyles, thereby highlighting the inherent evolutionary advantages of
26 this strategy.
27
28 Key words: Eusocial insects; Isoptera; Parthenogenesis; Reproduction; Selective purge; Sex
29 ratio; Sexual reproduction; Thelytoky.
2 Asexual queen succession in termites (A29115)
30 Key concepts
31 • The historical view of a lifelong monogamy between a primary queen and king in
32 termites now appears obsolete.
33 • Termite queens of some species combine the advantages of sexual and asexual
34 reproductions in a breeding system called Asexual Queen Succession.
35 • Asexual Queen Succession shapes the genomes of these species by the elimination of
36 recessive deleterious mutations through parthenogenetically-produced new queens.
37 • Asexual Queen Succession, along with the species’ ecology and lifestyle, influences
38 their population sex ratio.
39 • Variations in the modalities of Asexual Queen Succession indicate that its benefits are
40 used in a species-specific manner.
3 Asexual queen succession in termites (A29115)
41 Modes of reproduction
42 Reproduction is the ultimate purpose of all living organisms. Individuals are expected to
43 maximize their reproductive success, i.e. the number of copies of their genes passed on to the
44 next generation, especially through their own offspring. Therefore, why reproduce sexually
45 rather than asexually? All else being equal, sex has a twofold cost: populations of sexually
46 reproducing females suffer from the production of males which cannot reproduce by themselves
47 (cost of males), and reproduce at half the rate of asexual populations. This “Paradox of Sex”
48 (Williams 1975; Maynard Smith 1978) or “Queen of Problems” (Bell 1982) remains one of the
49 greatest enigmas in evolutionary biology. Advantages of sex generally outweigh these costs as
50 sexual reproduction is the rule for the vast majority of organisms. For example, only 0.1% of
51 insects obligately reproduce asexually (Normark 2014). See also: DOI:
52 10.1002/9780470015902.a0001716.pub2; DOI: 10.1002/9780470015902.a0028485.
53 Mating systems describe every process leading to reproduction, such as the modalities
54 of encountering the opposite sex, the number and sex of individuals involved (sex ratio,
55 monogamy, polygamy, mate choice), and how fertilization occurs (Kokko et al. 2014). While
56 reproduction can potentially be achieved by all individuals of a species, it is narrowed down to
57 a few in eusocial ones. Societies are considered eusocial upon reproductive division of labour
58 (i.e., the existence of reproductive and nonreproductive castes), overlapping generations of
59 adults, and cooperative care of the offspring (Wilson 1971). In insects, eusociality was reached
60 in termites and several hymenopteran lineages, two groups of major importance in ecosystems
61 (Hölldobler and Wilson 1990). In these, the modalities of reproduction mingled with the system
62 of castes can give rise to a true “biodiversity” of reproductive systems (Keller 2007). Notably,
63 some species with mixed modes of reproduction combine the advantages of sexual and asexual
64 reproductions (reviewed in Wenseleers and Van Oystaeyen 2011). In these systems, the
65 workforce is produced sexually while new queens arise from parthenogenesis. Workers
4 Asexual queen succession in termites (A29115)
66 therefore keep the potential to face environmental stress, while queens maximize the
67 transmission of their genes to the next generation. Such a strategy has been referred to as
68 “Conditional Use of Sex” in ants (Pearcy et al. 2004), and “Asexual Queen Succession” in
69 termites (Matsuura et al. 2009; Matsuura 2011). In this review, we will cover the occurrence of
70 parthenogenesis in termites, the phenomenon of Asexual Queen Succession, the prerequisites
71 to its evolution, as well as its consequences on the genetic and population characteristics of
72 species. See also: DOI: 10.1002/9780470015902.a0003670.pub3; DOI:
73 10.1002/9780470015902.a0022553; DOI: 10.1002/9780470015902.a0021907.pub2.
74 Parthenogenesis in termites
75 Termites (Isoptera) is a clade of cockroaches (Dictyoptera: Blattodea). They are all eusocial
76 and are the main animal decomposers of organic matter in tropical ecosystems (Holt and Lepage
77 2000). Karyotype studies have shown termites to be diplo-diploid and suggested a sex
78 determination mechanism based on heterochromosomes, males being heterogametic (reviewed
79 in Roisin 2001). It follows that parthenogenesis in termites is supposedly solely thelytokous,
80 i.e. limited to the production of females. As a comparison, in hymenopterans, males are haploid
81 and develop from unfertilized eggs, a process called arrhenotokous parthenogenesis. Queens of
82 social hymenopterans may thus be able to use both thelytoky and arrhenotoky to produce
83 females and males, respectively (for a review of modes of parthenogenesis in insects, see
84 Vershinina and Kuznetsova 2016). Thelytokous parthenogenesis has long been considered
85 facultative and anecdotal in termites, and seen as “making the best of a bad job” for colonies
86 initiated by female-female pairs (Matsuura and Nishida 2001). Occasional development of
87 unfertilized eggs (tychoparthenogenesis) was reported in a handful of termite species (Table 1),
88 as well as in their closest relatives, mantids and cockroaches (reviewed in Vershinina and
89 Kuznetsova 2016). It occurs through the occasional development of unfertilized eggs with
90 hatchlings typically suffering from low survival rates. The evolution of parthenogenesis is
5 Asexual queen succession in termites (A29115)
91 likely impeded by genetic and developmental constraints (reviewed in Engelstädter 2008). One
92 such constraint is to maintain ploidy levels. Another one is that oocytes, whose activation is
93 usually triggered by the sperm, should not be arrested during meiosis nor rely on other factors
94 usually provided by sperm for further development. Other possible constraints are genomic
95 imprinting through the lethal overexpression of some loci or the absence of expression of others,
96 and inbreeding depression due to the loss of heterozygosity inherent to some cytological modes
97 of ploidy restoration (see Genetic consequences of Asexual Queen Succession below). Once
98 these difficulties are overcome, conditional or obligate parthenogenesis can evolve (Simon et
99 al. 2003; Nozaki et al. 2018). As of now in termites, only some populations of the Japanese
100 kalotermitid Glyptotermes nakajimai are known to have evolved obligate parthenogenesis, with
101 the complete absence of males from societies (Yashiro et al. 2018). However,
102 tychoparthenogenesis seems to have evolved into facultative caste-dependent parthenogenesis
103 in a lot more species. See also: DOI: 10.1002/9780470015902.a0005791.pub2; DOI:
104 10.1002/9780470015902.a0028747.
105 Asexual Queen Succession
106 In termites, colonies are usually initiated by a pair of imagoes shedding their wings and
107 becoming (primary) queen and king, which will repeatedly mate together to produce the
108 members of the colony. This contrasts from the situation in social hymenopterans in which
109 males die shortly after mating, and whose queens store sperm for their entire life (reviewed in
110 Hartke and Baer 2011).
111 In most species, the primary queen and king can be replaced by neotenic reproductives
112 if they die (reviewed in Myles 1999). Neotenics are non-dispersing (secondary) reproductives
113 retaining juvenile traits and lacking imaginal features required for a dispersal flight —in
114 opposition to winged imagoes initiating new colonies. As neotenics take over reproduction in
115 their natal nest, various patterns of inbreeding may occur (father-daughter, mother-son, brother-
6 Asexual queen succession in termites (A29115)
116 sister). However, in a few species, the primary queen seems to die systematically before the
117 king: neotenic daughters produced by thelytokous parthenogenesis replace their mother and
118 mate with the primary king in their natal nest (see Figure 1), a process called asexual queen
119 succession (AQS) (reviewed in Matsuura 2017). Sterile castes (the workforce) as well as (most)
120 imagoes are produced through conventional sex. With such queen replacement, inbred matings
121 are avoided and genetic diversity is maintained, at least during the vast majority of the colony’s
122 life cycle (Figure 2; see Asexual Queen Succession and population sex ratio below). Compared
123 with the “Conditional Use of Sex” reported from ants, the fundamental difference involves the
124 use of sex in the genesis of dispersers founding new colonies: parthenogenesis mostly concerns
125 dispersing queens in ants and non-dispersing (neotenic) queens in termites. An exception is the
126 queen-polymorphic ant Vollenhovia emeryi, in which short-winged queens are
127 parthenogenetically-produced and disperse through nest budding, while long-winged ones arise
128 through sexual reproduction and initiate new colonies after a dispersal flight (Okamoto et al.
129 2015).
130 In species with AQS, queens therefore combine advantages of both sexual and asexual
131 reproductions. This breeding system also confers two advantages at the colony level. First, the
132 replacement of the primary queen by numerous queens increases the colony’s growth rate and
133 reproductive potential. Second, the consecutive replacement of queens within the nest expands
134 the colony’s lifespan. In turn, these features maximize the opportunities of colonies to
135 reproduce, i.e. of producing dispersers, which will initiate new colonies. Finally, AQS may
136 facilitate geographic expansion, as suggested by the wide distribution usually achieved by
137 species with such breeding system (Fougeyrollas et al. 2015; Fournier et al. 2016).
138 Independent origins of Asexual Queen Succession
139 AQS was initially described from the Japanese Rhinotermitidae Reticulitermes speratus
140 (Matsuura et al. 2009), and later found in two additional species of Reticulitermes (Vargo et al.
7 Asexual queen succession in termites (A29115)
141 2012; Luchetti et al. 2013). More recently, it was reported in several species of Termitidae
142 belonging to Syntermitinae and Termitinae subfamilies (Fougeyrollas et al. 2015; Fournier et
143 al. 2016; Fougeyrollas et al. 2017; Hellemans et al. 2019a). Because AQS occurs in
144 phylogenetically distant taxa, in contrasted ecological contexts —in temperate wood-feeding
145 subterranean Rhinotermitidae and in neotropical soil-feeding Termitidae— and under different
146 modalities of ploidy restoration (see Genetic consequences of Asexual Queen Succession
147 below), it appears clear that this breeding system evolved independently several times (Dedeine
148 et al. 2016; Matsuura 2017; Hellemans et al. 2019a). In addition to their occurrence in
149 contrasted ecological contexts, species with AQS also display various nesting habits: some
150 build their own nest while others are inquilines (i.e., species living in nests built by another
151 species; see Table 1). Little is understood about the selective pressures leading to the evolution
152 of AQS. In the case of inquiline species (see Table 1), one hypothesis is that cohabitation and
153 hostile interactions with the host may favour mechanisms of king and queen replacement
154 (Hellemans et al. 2019a). This ability for secondary reproduction (the production of neotenics)
155 is indeed a prerequisite to the evolution of this breeding system. In the case of the Syntermitinae
156 Silvestritermes minutus, fast queen replacement may have evolved to boost growth and alate
157 production —this species inhabiting small, soft-built, precarious nests with a short life
158 expectancy (Fougeyrollas et al. 2017). Whatever the selective pressures favouring its evolution,
159 the independent occurrences of AQS in species with contrasted cytological and ecological
160 backgrounds further highlight the inherent evolutionary advantages of this strategy.
161 Prerequisites to the evolution of Asexual Queen Succession
162 The evolution of AQS requires both the capacity to reproduce parthenogenetically
163 (tychoparthenogenesis) and the developmental propensity of parthenogens to develop into
164 neotenic queens (Nozaki et al. 2018). In termites, evidence points towards queens to be
165 intrinsically able to reproduce parthenogenetically, rather than induced by intracellular
8 Asexual queen succession in termites (A29115)
166 endosymbiotic bacteria (Matsuura et al. 2004; Yashiro and Lo 2019; Hellemans et al. 2019c).
167 At least in R. speratus, queens seem to possess an efficient mechanism ensuring
168 parthenogenesis with no possible interference from kings: they are able to lay eggs devoid of
169 micropyles (sperm gates), thereby preventing fertilization (Yashiro and Matsuura 2014). Caste
170 differentiation (e.g. the differentiation of an individual into a neotenic reproductive) in social
171 insects is the outcome of a complex continuum between heritable and socio-environmental
172 factors. The developmental priority of parthenogens to develop into neotenic queens can be
173 explained by genomic imprinting and the exclusive carry-over of queen-specific epimarks
174 (Matsuura et al. 2018). However, their achieved differentiation is also controlled by socio-
175 environmental factors: for instance, neotenic queens produce volatile pheromones suppressing
176 the differentiation of other queens in R. speratus (Matsuura et al. 2010). See also: DOI:
177 10.1002/9780470015902.a0028327.
178 Genetic consequences of Asexual Queen Succession
179 As mentioned above, inbred matings are avoided and genetic diversity is maintained upon
180 queen replacement by parthenogens. However, AQS has also more profound impacts on the
181 genomes of these species. Thelytoky can occur via two principal modes: apomixis through
182 which ploidy is maintained by mitosis and the resulting offspring are true clones of their
183 mothers, and automixis which involves meiosis followed by ploidy restoration. In termites,
184 apomixis was suggested in G. nakajimai (Yashiro et al. 2018), while species with AQS use
185 automixis. Furthermore, ploidy restoration under automixis occurs through different modalities
186 among AQS species: terminal fusion in species of Reticulitermes, central fusion in
187 Syntermitinae, and gamete duplication in Termitinae (Table 1). Each mode is characterized by
188 different rates of transition to homozygosity from the queen’s genotype (Figure 3). It follows
189 that in these cases, parthenogenetic daughters are not perfect clones of their mother, and are not
190 genetically identical to each other. Theoretically, conflict over reproduction among new queens
9 Asexual queen succession in termites (A29115)
191 may therefore occur, but whether it actually happens remains unknown (see also Asexual Queen
192 Succession and population sex ratio below). Finally, homozygosity exposes recessive
193 deleterious alleles to selection in parthenogens, and therefore AQS can be considered as a
194 purging system (Matsuura 2011). Because many replacement queens are produced, the purge
195 is achieved at low cost through the elimination and recycling of unfit individuals. This selective
196 purge is highly efficient in species restoring ploidy through gamete duplication, through which
197 fully homozygous individuals are produced. This efficiency is further evidenced by occasional
198 findings of parthenogenetically-produced primary queens in mature nests, i.e. nests producing
199 dispersers, of these species (Fournier et al. 2016; Hellemans et al. 2019a). This situation is
200 highly reminiscent of haplo-diploid organisms in which deleterious alleles are rapidly purged
201 through haploid males. See also: DOI: 10.1002/9780470015902.a0001359.pub3.
202 Asexual Queen Succession and population sex ratio
203 The occurrence of parthenogenesis and patterns of replacement of reproductives can also have
204 an impact on other features of the breeding system of these species, such as the sex ratio of
205 dispersers. Sex allocation, i.e. the production of dispersing sexuals rather than sterile castes, is
206 the ultimate goal of colonies. Sex ratio is the relative investment in males or females. Fisher's
207 (1930) theory predicts a 1:1 sex ratio in a population of diplo-diploid organisms if matings
208 occur at random, in the absence of both sexual competition and local resource competition. In
209 case of sexual dimorphism, sex ratio should deviate toward the cheapest sex in order to obtain
210 an equal (energetic) investment between males and females. Theory predicts the population sex
211 ratio to be evolutionary stable if the fitness gain per unit of investment into each sex is equal
212 from the viewpoint of the actors controlling the sex ratio (Bourke and Franks 1995). In termites,
213 the sex ratio could theoretically be controlled by the king through the male:female determining
214 cells in its sperm, by the queen through the male:female ratio of eggs laid (i.e., the primary sex
215 ratio), and by sterile helpers by biasing the investment towards the sex that better represents
10 Asexual queen succession in termites (A29115)
216 their genetic interests (i.e., the secondary sex ratio). See also: DOI: 10.1038/npg.els.0001745;
217 DOI: 10.1038/npg.els.0001719.
218 While the timing of replacement of the primary queen varies among AQS species, the
219 longer longevity of the primary king appears as a constant. The replacement of the primary
220 queen by parthenogenetically-produced neotenic daughters does not modify the genetic
221 architecture of the colony, as they only bear the genome of the primary queen (Figure 2a). This
222 is not the case upon the death of the primary king because he must be replaced by a neotenic
223 son produced through conventional sex, which bears half of the genome of the primary queen.
224 Mother-son inbreeding then occurs in the colony, and the genome of the primary queen is
225 transmitted three times more to the progeny than the one of the primary king. If such king
226 replacement is frequent in the population, females have a higher reproductive value than males
227 because they ultimately transmit more of their genes to the next generation. In these species, a
228 female-biased sex ratio, depending on the frequency of mother-son inbreeding, is expected at
229 the population level (Matsuura 2011; Kobayashi et al. 2013). Thus, this conditional
230 parthenogenesis inevitably provokes sexual conflict by depriving kings from genetic
231 contribution to the next generation (Yashiro and Matsuura 2014). See also: DOI:
232 10.1002/9780470015902.a0003669.pub3.
233 Accordingly, species of the genus Reticulitermes without AQS exhibit a balanced sex
234 ratio, while it is female-biased in species with AQS (Kobayashi et al. 2013; Luchetti et al.
235 2013). This is, however, not the case in AQS species from the Termitidae, whose sex ratio is
236 balanced (Fougeyrollas et al. 2017; Hellemans et al. 2019b). Interestingly, the differentiation
237 of parthenogens into neotenic queens is not perfectly hardwired in all species with AQS. For
238 instance, 18% of neotenic queens are produced sexually in the Termitinae Cavitermes tuberosus
239 (Fournier et al. 2016). If the primary king is still present, father-daughter inbreeding may occur,
240 thereby shifting the relative genetic contribution to the next generation in favour of the founding
11 Asexual queen succession in termites (A29115)
241 king (Figure 2b). Conversely, some female dispersers may also be produced asexually and
242 become successful foundresses, thereby raising the contribution of the founding queen to the
243 next generation. Furthermore, it is hypothesized that conflict over reproduction and sex ratio
244 may arise between parthenogenetically and sexually-produced neotenic queens as the former
245 ones are less related to the offspring of the latter ones (Hellemans et al. 2019b).
246 Finally, the magnitude of the bias will also be affected by the timing of queen and king
247 replacement as well as the life expectancy of such colonies, i.e. the proportion of generations
248 during which mother-son or father-daughter inbreeding occurs relative to those in which both
249 genomes are equally transmitted to the dispersers. In C. tuberosus, queen replacement seems to
250 be facultative and take place after colony maturity, thus at a late stage in the life cycle of the
251 colony compared to other species with AQS (Hellemans et al. 2019b). It follows that the life
252 expectancy of colonies may be short after queen replacement, and even shorter after queen and
253 king replacement, so that the proportion of generations with dispersers arising from mother-son
254 inbreeding might be low. The sex ratio expected in AQS species should therefore not be
255 systematically biased towards females, but depends on the interplay of various life history traits.
256 Conclusions and future directions
257 In summary, the historical view of a lifelong monogamy between a primary queen and king in
258 termites now appears obsolete, with an early (systematic) replacement of the primary queen in
259 species with the AQS breeding system or through the occurrence of obligate parthenogenesis
260 in female-only populations (Table 1). These conditional and obligate systems manifestly
261 evolved several times independently, as evidenced by the cytological biodiversity of ploidy
262 restoration and their occurrence in phylogenetically distant termite lineages. However, still little
263 is known on ecological determinants favouring the establishment of AQS as it evolved in
264 species with contrasted lifestyles, i.e. in nest-building species and inquilines, in temperate
265 xylophagous species as well as in neotropical humivorous ones (see Table 1). Moreover,
12 Asexual queen succession in termites (A29115)
266 variations in the reproductive origin of females (sexually-produced neotenic queens and
267 parthenogenetically-produced alates) and the modalities of queen replacement (timing, number
268 of neotenic queens) indicate that the benefits of AQS are used in a species-specific manner.
269 Nevertheless, such diverse evolutionary backgrounds and modalities highlight again the
270 inherent advantages of this reproductive strategy. In species with AQS, the longer longevity of
271 the primary king appears as a constant. In this line of evidence, several genes associated to
272 DNA repair were shown to be significantly upregulated in both somatic and reproductive tissues
273 of kings of R. speratus compared to queens (Tasaki et al. 2018). However, further studies are
274 warranted in order to understand how and why such asymmetry in longevity arose between
275 sexes in species with AQS, breaking lifelong monogamy.
13 Asexual queen succession in termites (A29115)
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355 pairs and female asexual units in the termite Reticulitermes speratus (Isoptera:
356 Rhinotermitidae). Population Ecology 43, 119–124. doi:10.1007/PL00012022
357 Matsuura, K., Vargo, E. L., Kawatsu, K., Labadie, P. E., Nakano, H., Yashiro, T., and Tsuji, K.
358 (2009). Queen succession through asexual reproduction in termites. Science 323, 1687.
359 doi:10.1126/science.1169702
360 Maynard Smith, J. (1978). ‘The Evolution of Sex’. (Cambridge University Press: Cambridge,
361 New-York.) doi:10.1016/0169-5347(90)90011-2
362 Myles, T. G. (1999). Review of secondary reproduction in termites (Insecta: Isoptera) with
363 comments on its role in termite ecology and social evolution. Sociobiology 33, 1–91.
364 Normark, B. B. (2014). Modes of reproduction. In ‘The Evolution of Insect Mating Systems’.
365 (Eds D. M. Shuker and L. W. Simmons.) pp. 1–19. (Oxford University Press: Oxford.)
366 Nozaki, T., Yashiro, T., and Matsuura, K. (2018). Preadaptation for asexual queen succession:
367 queen tychoparthenogenesis produces neotenic queens in the termite Reticulitermes
368 okinawanus. Insectes Sociaux 65, 225–231. doi:10.1007/s00040-018-0603-1
369 Okamoto, M., Kobayashi, K., Hasegawa, E., and Ohkawara, K. (2015). Sexual and asexual
370 reproduction of queens in a myrmicine ant, Vollenhovia emeryi (Hymenoptera:
371 Formicidae). Myrmecological News 21, 13–17. doi:10.1002/edn.93
372 Pearcy, M., Aron, S., Doums, C., and Keller, L. (2004). Conditional use of sex and
373 parthenogenesis for worker and queen production in ants. Science 306, 1780–1783.
374 Roisin, Y. (2001). Caste sex ratios, sex linkage, and reproductive strategies in termites. Insectes
375 Sociaux 48, 224–230. doi:10.1007/PL00001770
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376 Simon, J. C., Delmotte, F., Rispe, C., and Crease, T. (2003). Phylogenetic relationships between
377 parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals.
378 Biological Journal of the Linnean Society 79, 151–163. doi:10.1046/j.1095-
379 8312.2003.00175.x
380 Stansly, P. A. (1987). Parthénogenèse chez Velocitermes spp. (Isoptera: Nasutiterminae).
381 Comptes Rendus de l’Académie des Sciences de Paris (III) 304, 457–460.
382 Stansly, P. A., and Korman, A. K. (1993). Parthenogenic development in Velocitermes spp.
383 (Isoptera: Nasutiterminae). Sociobiology 23, 13–24.
384 Tasaki, E., Mitaka, Y., Nozaki, T., Kobayashi, K., Matsuura, K., and Iuchi, Y. (2018). High
385 expression of the breast cancer susceptibility gene BRCA1 in long‐lived termite kings.
386 Aging 10, 2668–2683. doi:10.18632/aging.101578
387 Vargo, E. L., Labadie, P. E., and Matsuura, K. (2012). Asexual queen succession in the
388 subterranean termite Reticulitermes virginicus. Proceedings of the Royal Society B 279,
389 813–819. doi:10.1098/rspb.2011.1030
390 Vershinina, A. O., and Kuznetsova, V. G. (2016). Parthenogenesis in Hexapoda: Entognatha
391 and non-holometabolous insects. Journal of Zoological Systematics and Evolutionary
392 Research 54, 257–268. doi:10.1111/jzs.12141
393 Wenseleers, T., and Van Oystaeyen, A. (2011). Unusual modes of reproduction in social
394 insects: shedding light on the evolutionary paradox of sex. BioEssays 33, 927–937.
395 doi:10.1002/bies.201100096
396 Williams, G. C. (1975). ‘Sex and Evolution’. (Princeton University Press: Princeton, US.)
397 Wilson, E. O. (1971). ‘The Insect Societies’. (Belknap Press: Cambridge.)
398 Xing, L.-X., Liu, M.-H., Kong, X.-H., Liu, X., Su, X.-H., Yin, L.-F., and Tan, J.-L. (2013).
399 Parthenogenetic reproductive behavior and initial colony foundation in the termite,
400 Reticulitermes aculabialis. Chinese Journal of Applied Entomology 50, 1671–1678.
18 Asexual queen succession in termites (A29115)
401 doi:10.7679/j.issn.2095-1353.2013.230
402 Yashiro, T., and Lo, N. (2019). Comparative screening of endosymbiotic bacteria associated
403 with the asexual and sexual lineages of the termite Glyptotermes nakajimai.
404 Communicative & Integrative Biology 12, 55–58. doi:10.1080/19420889.2019.1592418
405 Yashiro, T., Lo, N., Kobayashi, K., Nozaki, T., Fuchikawa, T., Mizumoto, N., Namba, Y., and
406 Matsuura, K. (2018). Loss of males from mixed-sex societies in termites. BMC Biology
407 16, 96. doi:10.1186/s12915-018-0563-y
408 Yashiro, T., and Matsuura, K. (2014). Termite queens close the sperm gates of eggs to switch
409 from sexual to asexual reproduction. Proceedings of the National Academy of Sciences of
410 the United States of America 111, 17212–17217. doi:10.1073/pnas.1412481111
411
19 Asexual queen succession in termites (A29115)
412 Further reading
413 Bignell, D. E., Roisin, Y., and Lo, N. (2011). ‘Biology of Termites: A Modern Synthesis’.
414 (Springer: Dordrecht, The Netherlands.) doi:10.1007/978-90-481-3977-4
415 Bourke, A. F. G. (2011). ‘Principles of Social Evolution’. (Oxford University Press: Oxford,
416 U.K.)
417 Hardy, I. C. W. (2002). ‘Sex ratios: Concepts and Research Methods’ Ed I. C. W. Hardy.
418 (Cambridge University Press: Cambridge.)
419 Matsuura, K. (2020). Genomic imprinting and evolution of insect societies. Population Ecology
420 62, 38–52. doi:10.1002/1438-390X.12026
421 Schön, I., Martens, K., and Van Dijk, P. (2009). ‘Lost Sex. The Evolutionary Biology of
422 Parthenogenesis’. (Springer.) doi:10.1007/978-90-481-2770-2
423 Suomalainen, E., Saura, A., and Lokki, J. (1987). ‘Cytology and Evolution in Parthenogenesis’.
424 (CRC Press: Boca Raton, Florida.)
20 Asexual queen succession in termites (A29115)
425 Glossary
426 Caste differentiation: The deviation from the imaginal pathway by immatures, leading to
427 morphologically and/or behaviourally specialized categories of individuals. In termites, it
428 designates the event of molting into sterile stages (workers, soldiers) or secondary reproductives
429 (neotenics).
430 Endosymbiont: Host-associated microorganism living in host cavities or intracellularly.
431 Reproductive value: For founders in social insects, the relative probability of male- versus
432 female-borne alleles to be transmitted to the next generation (through new founders). The
433 reproductive value is determined by the breeding structure: it is unbiased in outbred sexual
434 populations, but can become biased in case of parthenogenesis or inbreeding.
435 Selective purge: The elimination of deleterious recessive mutations from the gene pool through
436 exposition to selection.
437 Thelytokous parthenogenesis: The production of females from unfertilized eggs.
438 Tychoparthenogenesis: The occasional development of unfertilized eggs.
21 Asexual queen succession in termites (A29115)
439 Figures and Tables
440 Figure captions
441 Figure 1: Photographs of the humivorous Syntermitinae Silvestritermes minutus. (a) Primary
442 colony headed by a primary king (PK) and a primary queen (PQ). (b) Secondary colony headed
443 by the primary king and numerous parthenogenetically-produced neotenic queens. Two
444 generations of neotenic queens can be observed, younger ones with brown tergites and creamy
445 white intersegmental membranes (NQ1) and older ones more ochraceous overall, with lighter
446 tergites and darker intersegmental membranes (NQ2). Soldiers (S) and workers (W) are
447 produced sexually. Credits, Yves Roisin. Scale bars, 2 mm.
448
449 Figure 2: Simplified view of the consequences of reproductives’ replacements and modes of
450 reproduction (p, parthenogenesis; s, sexual reproduction) on the genetic structure of the colony
451 and the population through the asymmetric genetic contribution of the primary queen (in
452 orange) and king (in blue) to the next generation of colonies (based on data from the Termitinae
453 Cavitermes tuberosus). Workers, soldiers and (most) alates are produced sexually in all types
454 of colonies. (a) In a strict Asexual Queen Succession (AQS), the primary queen is replaced by
455 parthenogenetically-produced neotenic daughters, and no change in relative genetic
456 contribution of primaries to the offspring occurs. The later king replacement induces an
457 asymmetry of gene transmission among the primaries. If king replacement is frequent in the
458 population, females have a higher reproductive value (transmit more genes) than males, and a
459 female-biased sex ratio is expected in dispersers (future primaries). (b) The queen can also be
460 replaced by sexually-produced daughters, which leads to father-daughter inbreeding and more
461 king’s genes to be transmitted.
462
22 Asexual queen succession in termites (A29115)
463 Figure 3: Overview of the cytological mechanisms of ploidy restoration underlying automictic
464 parthenogenesis in termites, considering recombination during meiosis. In the case of gamete
465 duplication, either the haploid ootide divides and recombines, or duplicated chromosomes
466 remain in the original cell. In terminal fusion, the ootides resulting from the same secondary
467 oocyte re-unite. In central fusion, the two central polar nuclei produced from the two secondary
468 oocytes fuse. Recombination at a given locus depends on the distance from the centromere, and
469 the rate of transition to homozygosity (r) varies between modes: gamete duplication results in
470 full homozygosity, terminal fusion in homozygosity except for recombined loci, central fusion
471 in homozygosity for recombined loci only.
23 Asexual queen succession in termites (A29115)
472
473 Figure 1
24 Asexual queen succession in termites (A29115)
Early colony stage Dispersal flight Primary queen Primary king
Gene pool of the next p s generation of colonies (Alates) + Alates Neotenics Soldiers (Alates) Workers (Neotenics)
(a) Strict AQS Queen replacement (b) Father-daughter inbreeding
Neotenic queen (p) Neotenic queen (s)
p s p s
King replacement Colony life cycle and genetic structure genetic and cycle life Colony Neotenic king
p s
474 Differential transmission of female and male genomes in the population
475 Figure 2
25 Asexual queen succession in termites (A29115)
Primary oocyte
Meiosis
Ootides
Gamete duplication Terminal fusion Central fusion r = 1 r = 0.33 – 1 r = 0 – 0.33
476
477 Figure 3
26 Asexual queen succession in termites (A29115)
478 Table 1: Documented cases of thelytokous parthenogenesis in termites. Modified and updated
479 from Matsuura (2011).
Parthenogenesis Ploidy Family Species Distribution Ecology References (conditions) restoration Zootermopsis Facultative Archotermopsidae Nearctic Wood-nester Unknown Light (1944) angusticollis (laboratory) Zootermopsis Facultative Archotermopsidae Nearctic Wood-nester Unknown Light (1944) nevadensis (laboratory) Bifiditermes Facultative Kalotermitidae Oriental Wood-nester Unknown Chhotani (1962) beesoni (laboratory) Obligatory in some Glyptotermes Yashiro et al. Kalotermitidae Japan Wood-nester populations Unknown nakajimai (2018) (natural) Kalotermes Facultative Kalotermitidae Palaearctic Wood-nester Unknown Grassé (1949) flavicollis (laboratory) Neotermes Facultative Terminal Kobayashi and Kalotermitidae Oriental Wood-nester koshunensis (laboratory) fusion Miyaguni (2016) Reticulitermes Subterranean, Facultative Rhinotermitidae China Unknown Xing et al. (2013) aculabialis wood-feeder (laboratory) Reticulitermes Subterranean, Facultative, AQS Terminal Luchetti et al. Rhinotermitidae Palaearctic lucifugus wood-feeder (natural) fusion (2013) Reticulitermes Subterranean, Facultative Terminal Nozaki et al. Rhinotermitidae Japan okinawanus wood-feeder (laboratory) fusion? (2018) Reticulitermes Subterranean, Facultative, AQS Terminal Matsuura et al. Rhinotermitidae Oriental speratus wood-feeder (natural) fusion (2009) Reticulitermes Subterranean, Facultative, AQS Terminal Vargo et al. Rhinotermitidae Nearctic virginicus wood-feeder (natural) fusion (2012) Stansly (1987); Termitidae: Velocitermes Epigeal nests, Facultative Neotropical Unknown Stansly and Nasutitermitinae spp. litter-feeder (laboratory) Korman (1993) Termitidae: Embiratermes Epigeal nests, Facultative, AQS Fougeyrollas et Neotropical Central fusion Syntermitinae neotenicus humus-feeder (natural) al. (2015) Termitidae: Silvestritermes Epigeal nests, Facultative, AQS Fougeyrollas et Neotropical Central fusion Syntermitinae minutus humus-feeder (natural) al. (2017) Termitidae: Cavitermes Inquiline, Facultative, AQS Gamete Fournier et al. Neotropical Termitinae tuberosus nest-feeder (natural) duplication (2016) Termitidae: Inquilinitermes Inquiline, Facultative, AQS? Gamete Hellemans et al. Neotropical Termitinae inquilinus nest-feeder (natural) duplication? (2019a) Termitidae: Palmitermes Epigeal nests, Facultative, AQS Gamete Hellemans et al. Neotropical Termitinae impostor humus-feeder (natural) duplication (2019a) Termitidae: Spinitermes Inquiline, Facultative, AQS? Gamete Hellemans et al. Neotropical Termitinae trispinosus nest-feeder? (natural) duplication? (2019a) 480
481
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