Parthenogenesis in Fulgoromorpha and Cicadomorpha: History
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Subjects: Environmental Sciences
Contributor:
Dora Aguín-Pombo
,
Valentina G. Kuznetsova

Insects are renowned for their remarkable diversity of reproductive modes. Among these, the largest non-holometabolous order, Hemiptera, stands out with one of the most diversified arrays of parthenogenesis modes observed among insects. 

  • parthenogenesis
  • thelytoky
  • female-biased sex ratios
  • planthoppers
  • Delphacidae
  • leafhoppers
  • Cicadellidae

1. Introduction

The origin and evolution of parthenogenesis (parthenos = virgin, genesis = origin), a unique form of reproduction where embryonic development occurs in unfertilized eggs, have puzzled scientists for over a century. Parthenogenesis is a very common, naturally occurring phenomenon among many orders of the animal kingdom, especially invertebrates. The most comprehensive list to date of species reproducing parthenogenetically, as well as a discussion of modes of parthenogenesis in animals, was presented by Bell [1] (see [2][3][4][5][6]). Insects are known to have a wide variety of modes of reproduction and play a central role in our understanding of parthenogenesis, which is often referred to as either unisexual, uniparental, or asexual reproduction. Recently, reviews of known cases of parthenogenesis in different orders of insects have been published [7][8]. In total, parthenogenesis was found in 23 orders, including 2 orders of primary wingless insects, Microcoryphia (=Archaeognatha) and Zygentoma (=Thysanura s. str.), 13 orders of non-holometabolous insects (‘Hemimetabola’), and 8 orders of Holometabola, a monophyletic group that includes most insect species.
Parthenogenesis occurs in various forms and modes, among which the main ones are thelytoky (the mode where females produce only females from unfertilized eggs), arrhenotoky (females produce only males from unfertilized eggs), and deuterotoky (females produce both males and females from unfertilized eggs). Each of these strategies may appear in different groups in different varieties and via an obligatory or facultative manner. Most unisexual insect species or biotypes have arisen as a result of a mutation occurring within a bisexual population, through hybridization events, or by means of polyploidization. The majority of these unisexuals are polyploids, mainly triploids [9][10][11][12][13]. Finally, some endosymbiotic bacteria, most often Wolbachia Hertig 1936, can manipulate the reproductive strategy of the host and induce the transition to parthenogenesis [14][15].
The largest non-holometabolous insect order, Hemiptera (bugs), with approximately 97,000–103,590 known species [16][17], has the most diversified modes of unisexual reproduction among insects. The wide variety of reproductive modes and genetic systems of hemipterans make them suitable models for studying how unisexual reproduction emerges and how it is maintained across generations. Hemiptera are taxonomically divided into four monophyletic suborders, including Sternorrhyncha (scale insects, aphids, whiteflies, and psyllids; ~21 extant families), Heteroptera (true bugs sensu stricto; ~54 extant families), Coleorrhyncha (moss bugs or peloridiids; one extant family), Fulgoromorpha (planthoppers; ~20 extant families), and Cicadomorpha (leafhoppers, treehoppers, froghoppers, and cicadas; ~12 extant families) [18][19]. Existing studies show that parthenogenesis is unevenly distributed among and within these phylogenetic lineages. Moreover, trends in the evolution of unisexual forms exhibit significant disparities across different suborders [7][20].
The suborder Sternorrhyncha has the most notable instances and types of unisexual reproduction. This is especially true of scale insects (Coccoidea), in which bisexual reproduction is often combined with numerous aberrant modes of reproduction [21][22][23][24][25][26][27]. It is worth mentioning various modes of reproduction observed in scale insects, including haplodiploidy, diploid arrhenotoky with Paternal Genome Elimination (PGE; males are haploid) or Paternal Genome Heterochromatinization (PGH; males are diploid) during embryogenesis, automictic and apomictic thelytoky (both obligate or facultative), deuterotoky, and hermaphroditism, which is in fact extremely rare in insects. Most aphids (Aphidoidea) typically reproduce by cyclical parthenogenesis, alternating one annual (sometimes biannual) bisexual generation with several (or numerous) unisexual (all-female) generations reproducing by apomictic parthenogenesis. The bisexual generation may be lost secondarily, so that reproduction is then exclusively by thelytoky [28][29][30][31][32][33][34]. Although very little is known about the genetic makeup of whiteflies (Aleyrodoidea), it has been shown in some model species (e.g., Bemisia tabaci (Gennadius, 1889) and Aleurodicus rugioperculatus Martin, 2004) that the females are derived from fertilized eggs, whereas males are parthenogenetically produced by arrhenotoky [35][36]. In this system, males inherit their mother’s but not their father’s genes. Psyllids (Psylloidea) are almost exclusively bisexual. However, some species are known to reproduce by parthenogenesis, at least in separate populations [37][38], and the issue of parthenogenesis in these species, its origin, and its evolutionary role have been the subject of many articles in recent years (e.g., [39][40][41][42]). There are no known cases of unisexual reproduction in peloridiids (Coleorrhyncha), and only a few thelytokous (most likely facultatively thelytokous) species have been reported in true bugs (Heteroptera) [43][44].

2. A Brief History of Parthenogenesis in Fulgoromorpha and Cicadomorpha

The suborders Fulgoromorpha and Cicadomorpha, previously grouped in the suborder Auchenorrhyncha, are two worldwide specious groups with more than 43,000 valid species [45][46] distributed roughly in 32 families. Fulgoromorpha contain one superfamily, Fulgoroidea, with 20 recognized families, and Cicadomorpha include the superfamilies Cicadoidea (cicadas, 2 families), Cercopoidea (spittlebugs, 5 families recognized here, but 3 in Hamilton [47]), and Membracoidea (leafhoppers and treehoppers, 5 families).

The history of parthenogenesis in Auchenorrhyncha began with experimental studies on the American species of leafhoppers, Agallia quadripunctata (Provancher, 1872) (Cicadellidae, Agallinae, Agalliini), in which different populations consist predominantly of females ([48] and references therein). Since the mid-1970s, a group of scientists from the Agricultural University of Wageningen (The Netherlands), including S. Drosopoulos, C.J.H. Booij, A.J. De Winter, P.W.F. De Vriejer, and C.F.M. Den Bieman, has made significant contributions to the study of parthenogenesis in Auchenorrhyncha. Drosopoulos [49][50] followed by Den Bieman and Eggers-Schumacher [51] and Den Bieman [52][53][54] showed that planthoppers of the genera Muellerianella Wagner, 1963, and Ribautodelphax Wagner, 1963 (both from the family Delphacidae, Delphacinae), reproduce by pseudogamy. Den Bieman and de Vrijer [55] were the first to describe a case of true parthenogenesis in the planthopper genus Delphacodes Fieber, 1866 (Delphacidae, Delphacinae, Delphacini). This group of researchers continued to work intensively over the next 15 years with a multidisciplinary approach that involved studies on morphology, cytogenetics, population genetics, hybridization, mating acoustic communication, ecology, and distribution. More recently, true parthenogenesis has been documented for the leafhopper genus Empoasca Walsh, 1862 (Cicadellidae, Typhlocybinae, Empoascini) from Madeira Island, where three apomictic morphotypes have been discovered and extensively studied [56][57]. A recent study [58] suggested that the sex-distorting bacteria of the genus Rickettsia da Rocha-Lima, 1916 could be responsible for the origin of parthenogenesis in these leafhoppers. There are other published records of bisexually reproducing Auchenorrhyncha species. In these cases, vertically transmitted endosymbiotic bacteria belonging to the genera Wolbachia, Cardinium Zchori-Fein et al. 2004, Arsenophonus Gherna et al. 1991, Spiroplasma Saglio et al. 1973, and Rickettsia—collectively referred to as reproductive parasites—induce a shift in the sex ratio towards females. These infections compel infected females to produce offspring daughters in the absence of mating (e.g., [59][60]). In addition, in some species, parthenogenesis is suspected only because there is a bias towards females or a complete absence of males in the field collections (e.g., [61]).

3. A Brief Overview of the Patterns and Origins of True Parthenogenesis

Strictly speaking, parthenogenesis refers to reproduction by virgin females. That is, females give rise exclusively to females without the need for mating. This type of parthenogenesis, known as true parthenogenesis, can manifest in two forms: obligatory parthenogenesis and facultative parthenogenesis. In the first case, species reproduce solely by parthenogenesis, while in the second case, parthenogenesis is a sporadic means of reproduction. A particular case of facultative parthenogenesis, termed cyclical parthenogenesis, is when the sexual and asexual modes of reproduction alternate according to environmental conditions [6]. This mode of reproduction is very common in Sternorrhyncha, specifically in aphids, while in Cicadomorpha and Fulgoromorpha, obligate parthenogenesis is the only type so far reported. Depending on whether new parthenogenetic forms arise from unfertilized eggs that have undergone or not meiosis, true parthenogenesis can be further divided into automictic and apomictic, respectively. Furthermore, based on the sex produced by parthenogenesis, a distinction is made between arrhenotoky (producing only males), thelytoky (producing only females), and deuterotoky or amphitoky, where eggs develop both into males and females [6]. In thelytoky, offspring can be diploid, triploid, or polyploid, though triploidy is the more common form. In most cases of thelytokous parthenogenesis, eggs do not suffer chromosome reduction through meiosis (apomixis); nonetheless, in some groups, meiotic reduction of genetic material is followed by a subsequent restoration of diploidy in offspring (automixis) [62].

There are three primary origins of thelytoky [10][63]. The first of these is associated with hybridization, i.e., crosses between two bisexual species resulting in the generation of parthenogenetic hybrids. The second origin has to do with genetic mutations, i.e., spontaneous loss of “sexual” reproduction due to mutations in genes responsible for the production of bisexual forms and the successful occurrence of meiosis. The third origin is associated with bacterial endosymbiosis, specifically infection by inherited bacteria capable of invading the host species and sustaining their presence by manipulating the reproduction of infected hosts. In the last decades, due to advances in microbiology, it has been discovered that symbionts of the Flavobacterium clade, such as Wolbachia, Cardinium, Arsenophonus, and Spiroplasma, and the Rickettsia clade, can be reproductive parasites [64][65]. Notably, in the majority of cases, it is Wolbachia that has been suggested to infect over 70% of arthropod species [66], including more than a million insect species [14]. Bacterial endosymbionts live inside the cytoplasm in reproductive tissues. To increase the proportion of infected females, they can modify the reproductive biology of the host, skewing the sex ratio towards females. In different insects, host reproduction can be affected by the induction of parthenogenesis, feminization of males, male killing, and the induction of cytoplasmic incompatibility between gametes (CI), a form of embryonic lethality in crosses between males and females with different infection status [15]. In Auchenorrhyncha, the effects of these bacteria on reproductive biology have been studied in only a few species; however, they have been shown to cause phenomena such as CI, male killing, and feminization of males [59][60][67][68][69][70][71]. A recent study [58] suggested that Rickettsia might induce parthenogenesis in the leafhopper genus Empoasca.

This entry is adapted from the peer-reviewed paper 10.3390/insects14100820

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