Evolution of Asexual Queen Succession System in Termites
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綜合論述 台灣昆蟲 31: 117-131 (2011) Formosan Entomol. 31: 117-131 (2011) Evolution of Asexual Queen Succession System in Termites Kenji Matsuura* Laboratory of Insect Ecology, Graduate School of Environmental Science, Okayama University, Okayama 700-8530, Japan ABSTRACT The evolution and maintenance of sexual reproduction is believed to involve important tradeoffs. The queens of social insects are faced with a dilemma over the costs and benefits of sexual and asexual reproduction. Asexual reproduction by a queen doubles her contribution to the gene pool. However, overuse of asexual reproduction reduces the genetic diversity of the offspring and thus the ability of the colony to adapt to environmental stress. Recent research suggests that queens of some Reticulitermes termites can solve this tradeoff by the conditional use of sexual and asexual reproduction, whereby queens produce neotenic (secondary) queens by parthenogenesis but use sexual reproduction to produce workers and alates (sexual imagos). I also discuss proximate physiological mechanism and genetic background of the asexual queen succession system in the termites. Key words: thelytoky, caste differentiation, genetic diversity, queen succession, queen pheromone, sex ratio Introduction altruistic members. Hughes et al. (2008) compared female mating frequencies in Kin selection and inclusive fitness eusocial Hymenoptera and demonstrated theory predicts that high relatedness, that monandry was the ancestral state possibly generated by genetic factors such when eusociality arose in Hymenoptera as haplodiploidy, inbreeding, or clonal and that mating by queens with multiple reproduction, is critical to the evolution of males is always derived. High levels of eusociality. However, relatedness among polyandry occur only in species whose workers within colonies of some species is workers have lost reproductive totipotency. relatively low due to sexual reproduction, Similarly, polygyny is also derived. This including outbreeding, multiple mating indicates that high relatedness has played (polyandry), and multiple reproductive a decisive role in the evolution of eusociality females (polygyny), which lowers the and strongly supports inclusive fitness potential inclusive fitness gains for theory. *Corresponding email: [email protected] Evolution of Asexual Queen Succession System in Termites 117 Living in social groups has not only has been regarded as an unusual case advantages but also drawbacks. For example, with little adaptive significance in nature. infectious diseases can potentially spread Even after the adaptive significance of more easily among group members than termite parthenogenesis was recognized, solitary-living individuals. Transmission is researchers believed that the function of more likely in groups because individuals parthenogenesis in termites was no more live at high densities and have frequent than “the best of a bad job”, that is, social contact. In addition, group members females used parthenogenesis only when are close relatives and thus susceptible to they failed to mate with males (Matsuura the same parasite infections (Schmid- and Nishida, 2001; Matsuura et al., 2002). Hempel, 1998). This can be understood Most recently, however, it was revealed using an analogy to human agriculture that parthenogenesis in some termite (e.g., Muira et al., 2008). Selective breeding species plays a much greater role than has of crops for desirable traits and against been previously understood. In the Japanese the undesirable ones leads to monocultures, subterranean termite R. speratus (Matsuura or entire farms of nearly genetically identical et al., 2009) and the North American plants. Little to no genetic diversity makes subterranean termite R. virginicus (Matsuura crops extremely susceptible to widespread and Vargo, in prep.), queens exclusively disease. Low genetic variance and closely use parthenogenesis to produce secondary spaced individuals may be the reasons (neotenic) queens. On the other hand, why the avian flu causes devastating queens produce workers and alates by effects on poultry farming and why plant outcrossing with the primary king. This hoppers wipe out acres of rice paddies at model of asexual queen succession (AQS) once. Both human agriculture and social or conditional use of sexual and asexual insect colonies face risks associated with reproduction can be studied to understand high density and low genetic diversity. the advantages and disadvantages of Perhaps the best solution to the thelytoky in termites. dilemma over the costs and benefits of sexual and asexual reproduction is to use Thelytoky in eusocial insects both modes of reproduction conditionally Thelytoky is a type of parthenogenesis and therefore to experience the advantages in which females are produced from of both. Indeed, recent studies have unfertilized eggs. Among the 12,500 ant uncovered unusual modes of reproduction and 2,400 termite species in the world, both in the ants Cataglyphis cursor (Pearcy thelytoky has been reported in only nine et al., 2004), Wasmannia auropunctata ant species and seven termite species. (Fournier et al., 2005), and Vollenhovia Thus, the percentages of species with emeryi (Ohkawara et al., 2006), and in the thelytokous capability are 0.07% and termite Reticulitermes speratus (Matsuura 0.29% in ants and termites, respectively. et al., 2009), in which advantage is taken These values are much lower than 2%, of the social caste system to use sex for which is the percentage of all insect somatic growth, but parthenogenesis for species with thelytokous capabilities. By germ line production. taking advantage of asexual reproduction, The capability of parthenogenesis in queens of eusocial insects are able to Isoptera was first reported by Light in realize a twofold advantage over sexual 1944. However, the reproductive biology of reproduction by allowing the transmission termite parthenogenesis has not been of twice the number of genes to offspring. examined in detail beyond its notional This leads to the very interesting question documentation until recently. This is of why thelytoky is so rare among eusocial largely because parthenogenetic reproduction insects. 118 台灣昆蟲第三十一卷第二期 One possible explanation is that only Reticulitermes termites have a fixed a limited number of studies have carefully number of chromosomes (2n = 42). examined the possibility of thelytokous Karyotypic chromosome observations showed parthenogenesis in eusocial insects. that parthenogenetic offspring are diploid, Thelytoky may be more difficult to detect with 2n = 42 chromosomes in R. speratus. in eusocial insects than in other insects Although termite sex determination mecha- because its presence is sometimes concealed nisms are not completely understood, or suppressed by social structure; the males commonly appear heterogametic in mechanisms that cause this are described termites (Roisin, 2001). Interchange multiples in the next section. Indeed, findings by L. (chains or rings of chromosome) in the Keller of the conditional use of asexual male meiosis is common in termites reproduction in ants arose by pure (Syren and Luykx, 1977). Chromosome serendipity (Keller, 2007). Future studies multivalents have been observed in male may reveal thelytoky in many more meiosis in R. speratus, generating a eusocial species. Possibly the rarity of multiple-X, multiple-Y system (Matsuura, thelytoky in eusocial insects is attributable 2002). Because of the XY sex determi- to the importance of genetic diversity nation system, termite parthenogenesis among colony members. While asexual produces only female progeny. reproduction by a queen would increase The genotypes of parthenogenetic within-colony relatedness, the resulting offspring depend on the mode of partheno- reduction in genetic diversity within genesis (Templeton, 1982). Thelytokous colonies would lower homeostasis in colonies. parthenogenesis can be categorized into For example, low genetic diversity colonies two major cytological divisions, “apomixis are more afflicted by disease than (ploidy stasis)” and “automixis (ploidy genetically diverse colonies in bumblebees restoration).” In apomictic partheno- (Baer and Schmid-Hempel, 2001), honeybees genesis, known as clonal reproduction in (Seeley and Tarpy, 2007) and leaf-cutting aphids, the features of meiosis are either ants (Hughes and Boomsma, 2004). In entirely or partially lacking. Only one honeybees, high-diversity colonies maintain maturation division takes place in the egg more uniform temperatures in their brood and this division is equational. The nests than did the uniform ones due to a offspring retain the genetic constitution of system of genetically based task speciali- the mother (excluding mutations), and zation (Jones et al., 2004). Thus, reduction heterozygosity is maintained in subse- in genetic diversity would render the quent generations. colonies less resilient to environmental Importantly, parthenogenesis of termites perturbation. A comprehensive survey of is not clonal. Thelytoky in termites, such species capable of thelytokous partheno- as R. speratus and R. virginicus, is genesis is a necessary next step in the accomplished by automixis with terminal effort to understand the costs and benefits fusion, in which two haploid pronuclei that of sexual and asexual reproduction for divide at meiosis ΙΙ fuse (Fig.1). Thus, eusocial insects. offspring are homozygous for a single maternal allele at all loci that did not Mechanism of termite parthenogenesis crossover,