Antiplacentas and Incestuous Teratomata: Reproductive Weirdness among the Coccoids

Gynandromorph of Papilio glaucus (M=L/F=R), photographed by James Adams

A valid dictum of biology could be that for nearly every law, as per a field like physics or mathematics, there will be at least one exception. One of these "laws" is that the Insecta are strictly dioecious: that is, male and female gametes are never produced by the same individual. Teratogenic exceptions are of course sometimes documented (of which bilateral gynandromorphs are the most visually notable), but the sheer rarity of hermaphroditic hexapods is striking, particularly when one considers that the frequency of this phenomenon throughout the rest of the Pancrustacea* (Juchault, 1999; Normark, 2002) and Metazoa as a whole.

Cluster of Icerya purchasi photographed by Colette Micallef (host plant unspecified)

Indeed, the only known hermaphroditic insects are three species in the economically significant coccoid genus Icerya (Hemiptera: Sternorrhyncha: Coccoidea: Monophlebidae), including I. purchasi, the cottony cushion scale of agricultural infamy (Royer, 1975). Phylogenetic inferences imply that these lineages each independently developed hermaphroditism (Unruh & Gullan, 2008). However, the often-cited factoid of hermaphroditic monophlebids does not hold up to developmental scrutiny: the reality of reproduction in these Icerya spp. is far more peculiar.

You thought that the life cycle of Micromalthus debilis was complicated? Get a load of this

Unprepossessing but speciose, the Coccoidea as a whole are remarkable for a trend towards paedomorphy and immobility among females, with males correspondingly becoming minute and non-feeding. They are even more remarkable in that this one clade encapsulates the entire diversity of sexual systems known in the Insecta (Ross et al., 2012), with the supposed ancestral condition of sex determination being XX-XO (see flowchart of transitions between these character states at left from Ross et al., 2010), but in several lineages of Icerya, sex determination is haplodiploid: males develop from unfertilized (haploid) eggs, whereas females are diploid (Ross et al., 2010). This fact is integral to comprehending the reproductive realities of these putative hermaphrodites. 

In I. purchasi, males are rare but not unknown; the bulk of the population (>90%) consists of self-fertilizing "hermaphrodites" in functional terms, but females in fact (Hughes-Schrader, 1925), with spermatozoa produced by haploid tissue (Royer, 1975). In the case of I. purchasi, at least, this haploid tissue is established from excess parental sperm, which, rather than fertilize oocytes, establish themselves transovarially in female oocysts and proliferate within diploid female tissues. As Normark (2003) put it, "hermaphroditism may be an inadequate term with which to describe this situation." Rather, female cottony cushion scales are infected with a vertically-transmitted clonal lineage of males reduced to a germ line. I. purchasi females breed with this "permanent cancer of the[ir] germ line" (Normark, 2003), which due to the lack of recombination inherent in haploid males' conception is (in genetic terms) their own father incarnate as a teratoma.

Schematic of reproductive possibilities in hermaphroditic Icerya spp. (Gardner & Ross, 2011)

While bizarre, this arrangement need not require a listen to the original soundtrack to "Annihilation" (2018) and a hallucinogenic drug of one's choice to make adaptive sense. (Although both actions are appropriate responses.) From an inclusive-fitness perspective, the male germlines of Icerya maximize their fitness by cloning themselves and obligately inbreeding with their female descendants (Gardner & Ross, 2011), with scope for both competition and collaboration between females and infectious male tissues.

Icerya does not contain the only examples of dizygotic (Gavrilov & Kuznetsova, 2007) tissue in coccoids, although the other two examples have an entirely separate adaptive justification: namely, to vertically transmit bacteriomes, a descriptive term referring to specialized tissues (consisting of bacteriocytes) that withhold endosymbionts. In Sternorrhyncha, it is generally assumed that these bacteria provide essential amino acids absent from a diet (plant sap) that consists almost exclusively of polysaccharides (Thao et al., 2002). In the monobasic (Hodgson and Hardy, 2013) Putoidae, which unlike Icerya are diplodiploid (Hughes-Schrader, 1944), maternal bacteriocytes invade the nascent embryo and propagate therein, bacteria and all (Buchner, 1965), thus giving rise to a bacteriome of maternal tissue. Cytogenesis that has dizygotic products is termed Schrader fusion (Gavrilov & Kuznetsova, 2007).

β-(blue) and γ-(red) proteobacteria, both without (L) and within (R) Planococcus citri oocyte

Conversely to the Putoidae, the Diaspididae (Gavrilov & Kuznetsova, 2007) and at least some true mealybugs (Pseudococcidae) engage in Schrader fusion involving the oocyte's polar bodies (which degenerate in the remainder of the Metazoa), again as a means of creating bacteriomes (Normark, 2003). Typical mealybugs host β-proteobacterial endosymbionts (Candidatus† Tremblaya princeps in Pseudococcinae, Candidatus T. phenacola in Phenacoccinae; López-Madrigal et al., 2015) (contrasting with the γ-proteobacteria that generally act in this digestive context throughout the Insecta; Moran & Telang, 1998). In many Pseudococcinae, T. princeps may in turn host γ-proteobacteria (Candidatus Moranella endobia) that provide essential amino acids for the β-proteobacterium (an interesting tale of genome reduction that is well beyond the scope of this post; López-Madrigal et al., 2015). Polar bodies invade the developing egg, apparently fuse with energids‡, and are then colonized (Schrader, 1922) by these endosymbiotic bacterial consortia (López-Madrigal et al., 2013), as shown above (von Dohlen et al., 2001).

Diagram of diaspidid life cycle; note triploidy of polar body that undergoes Schrader fusion (Normark, 2004)

Normark (2003) calls such tissues antiplacentas, although this term is somewhat disingenuous. Rather than being extensions of the offspring's zygote that remain within maternal bodies for the remainder of her life, and is indeed essential to the mother's survival, placentas are immediately dispensable things. A comparison to the triploid endosperm of Anthophyta (flowering plants) seems more apt (Gavrilov & Kuznetsova, 2007), as pseudococcid bacteriomes are polyploid due to their origin.

Why the multiple dizygotic systems cited above? And why among the Coccoidea alone does this occur, among all the diversity that is the Metazoa? To be brief, we do not know. Normark (2004) hypothesizes that polar body-based Schrader fusions act to conceal the sex of offspring from endosymbionts, which due to strictly vertical transmission are incentivized to skew sex ratios towards females. In this scenario, Schrader fusion results from genetic conflict between mutualistic symbionts. However, experimental work is required for any substance to attach to this intriguing idea.


*A term for the clade including the Hexapoda, and the "Crustacea" from within which the hexapods descend.
†A category into which a confirmed bacterial taxon can be placed pending formal description.
‡Nuclei in a proliferating embryo that have not undergone cleavage, such that they are surrounded by distinct halos of cytoplasm but have no cell walls.

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Buchner, P. (1965). Endosymbiosis of Animals with Plant-Like Micro-Organisms. New York: Wiley. 

von Dohlen, C. D.; Kohler, S.; Alsop, S. T.; and McManus, W. R. (2001). Mealybug β-proteobacterial endosymbionts contain γ-proteobacterial symbionts. Nature, 412, 433-436.

Gardner, A. and Ross, L. (2011). The evolution of hermaphroditism by an infectious male-derived cell lineage: an inclusive-fitness analysis. The American Naturalist, 178(2), 191-201.

Gavrilov, I. A. and Kuznetsova, V. G. (2007). On some terms used in the cytogenetics and reproductive biology of scale insects (Homoptera: Coccinea). Comparative Cytogenetics, 1(2), 169-174.

Haig, D. (1993). The evolution of unusual chromosomal systems in coccoids: extraordinary sex ratios revisited. Evolutionary Biology, 6(1), 69-77.

Hodgson, C. J. and Hardy, N. B. (2013). The phylogeny of the superfamily Coccoidea (Hemiptera: Sternorrhyncha) based on the morphology of extant and extinct macropterous males. Systematic Entomology, 38(4), 794-804.

Hughes-Schrader, S. (1925). Cytology of hermaphroditism in Icerya purchasi (Coccidae). Cell and Tissue Research, 2(2), 264-290.

Hughes-Schrader, S. (1944). A primitive coccid chromosome cycle in Puto sp. The Biological Bulletin, 87(3), 167-176.

Juchault, P. (1999). Hermaphroditism and gonochorism: a new hypothesis on the evolution of sexuality in Crustacea. Comptes Rendus de l'Académie des Sciences - Series III - Sciences de la Vie, 5, 423-427.




López-Madrigal, S.; Balmand, S.; Latorre, A.; Heddi, A.; Moya, A.; and Gil, R. (2013). How Does Tremblaya princeps Get Essential Proteins from Its Nested Partner Moranella endobia in the Mealybug Planoccocus citri? PLOS ONE, 8(10), e77307.

López-Madrigal, S.; Latorre, A.; Moya, A.; and Gil, R. (2015). The link between independent acquisition of intracellular gamma-endosymbionts and concerted evolution in Tremblaya princeps. Frontiers in Microbiology, 6(642), 1-10.



Moran, N. A. and Telang, A. (1998). Bacteriocyte-associated symbionts of insects: a variety of insect groups harbor ancient prokaryotic endosymbionts. BioScience, 48, 295-304.  

Normark, B. B. (2003). The evolution of alternative genetic systems in insects. Annual Review of Entomology, 48, 397-423.

Normark, B. B. (2004). The strange case of the armored scale insect and its bacteriome. PLOS Biology, 2(3), e43.

Ross, L.; Pen, I.; and Shuker, D. M. (2010). Genomic conflict in scale insects: the causes and consequences of bizarre genetic systems. Biological Reviews, 85(4), 807-828.

Ross, L.; Shuker, D. M.; Normark, B. B.; and Pen, I. (2012). The role of endosymbionts in the evolution of haploid-male genetic systems in scale insects (Coccoidea). Ecology and Evolution, 2(5), 1071-1081.

Royer, M. (1975). Hermaphroditism in insects: studies on Icerya purchasi. In Reinboth, R. (ed.): Intersexuality in the Animal Kingdom (pp. 135-145). Berlin: Springer.

Schrader, F. (1922). The sex ratio and oogenesis of Pseudococcus citri. Molecular and General Genetics, 30, 163-182.

Thao, M. L.; Gullan, P. J.; and Baumann, P. (2002). Secondary (γ-Proteobacteria) Endosymbionts Infect the Primary (β-Proteobacteria) Endosymbionts of Mealybugs Multiple Times and Coevolve with Their Host. Applied Environmental Microbiology, 68(7), 3190-3197. 
 
Tremblay, E. and Caltagirone, L. E. (1973). Fate of polar bodies in insects. Annual Review of Entomology, 18, 421-444. 

Unruh, C. and Gullan, P. (2008). Molecular data reveal convergent reproductive strategies in iceryine scale insects (Hemiptera: Coccoidea: Monophlebidae), allowing the reinterpretation of morphology and a revised generic classification. Systematic Entomology, 33, 8-50.