CLASSIFICATION OF THE MAJOR GENETIC SYSTEMS OF INSECTS http://www.annualreviews.org/doi/suppl/10.1146/annurev.ento.48.09180...

Supplemental Material: Annu. Rev. Entomol.2003.48:397-423.

doi: 10.1146/annurev.ento.48.091801.112703

Benjamin B. Normark, The Evolution of Alternative Genetic Systems in Insects

CLASSIFICATION OF THE MAJOR GENETIC SYSTEMS OF INSECTS

This longer version of the classification is nonetheless still simplified and somewhat arbitrary.
Many different classifications are possible. A more complete classification would cover the
various mechanisms of sex determination under amphimixis (5-7); different mechanisms of
automixis (23, 36); minor genetic systems, such as the diploid arrhenotoky of some scale
insects (30); and extrazygotic inheritance.

I. Obligate amphimixis (sex, sexuality). Every female inherits one haploid genome from
her mother and one haploid genome from her father.

A) Diplodiploidy (diploid-male systems). Every male inherits one haploid genome

from his mother and one haploid genome from his father, and these two haploid
genomes have equal probability of transmission through his sperm. Found in large
majority of all insect species; ancestral system in all orders except Thysanoptera and
Hemiptera.

B) Haplodiploidy (haploid-male systems, male haploidy, uniparental-male

systems). A male transmits only his mothers genome.

1) Arrhenotoky. Every male develops from an unfertilized egg and has only a
haploid genome inherited from his mother. Found (25, 29) in Thysanoptera
(all), Hymenoptera (all), Hemiptera (all Aleyrodidae, iceryine Margarodidae),
Coleoptera (Micromalthidae, xyleborine Curculionidae).

2) Paternal genome elimination (PGE, paternal genome loss). Every male

develops from a zygote containing one haploid genome from his mother and
one haploid genome from his father, but only the maternal genome is
transmitted through his sperm (19).

a) Embryonic PGE (pseudoarrhenotoky, parahaplodiploidy). In males,

the paternal genome is eliminated early in embryogenesis. Adult males
are haploid. Found in Hemiptera (some Diaspididae).

b) Germline PGE (functional haplodiploidy). In males, the paternal

genome is present in all tissues but eliminated during spermatogenesis
and not transmitted. Found in Hemiptera (most Coccoidea), Coleoptera
(Hypothenemus), and Diptera (Sciaridae).

II. Thelytoky (all-female systems, uniparental reproduction, parthenogenesis). A female

1 of 6 11/11/2017, 5:45 PM
CLASSIFICATION OF THE MAJOR GENETIC SYSTEMS OF INSECTS http://www.annualreviews.org/doi/suppl/10.1146/annurev.ento.48.09180...

transmits only her mothers genome; no sons are produced, only daughters.

A) Thelytokous parthenogenesis. No mating occurs. There are no males.

1) Apomixis (ameiotic parthenogenesis, strict clonality). Eggs are produced

mitotically. Found (36) in scattered species of Orthoptera (Tettigoniidae),
Phasmatodea (Heteronemiidae), Embioptera (Oligotomidae), Blattodea
(Blaberidae), Hemiptera (Aphididae, Margarodidae, Coccidae,
Pseudococcidae, Diaspididae, Delphacidae), Coleoptera (Chrysomelidae,
Curculionidae), Hymenoptera (Tenthredinidae), Diptera
(Chironomidae,Psychodidae, Simuliidae, Agromyzidae, Chamaemyiidae).

2) Automixis (meiotic parthenogenesis). Meiosis occurs, but ploidy of eggs is

restored through any of various mechanisms, reviewed in Suomalainen et al.
(36) and Lamb and Willey (23). Found (36) in scattered species of Orthoptera
(Eumastacidae, Rhaphidiphoridae), Phasmatodea (Bacillidae, Phasmatidae),
Thysanoptera (Thripidae), Hemiptera (Aleyrodidae, Margarodidae,
Pseudococcidae, Coccidae, Diaspididae), Coleoptera (Anobiidae),
Hymenoptera (Tenthredinidae, Aphelinidae, Cynipidae, Diprionidae,
Ichneumonidae), Lepidoptera (Psychidae), and Diptera (Lonchopteridae,
Drosophilidae).

B) Sperm-dependent thelytoky (obligate mating). Mating (with males of a related

amphimictic population) is necessary to initiate development.

1) Pseudogamy (gynogenesis). Sperm activate development but the sperm

nucleus does not fuse with the egg nucleus. Only maternal genes are
transmitted to offspring (all daughters).

a) Apomictic pseudogamy. Known in Hemiptera (Delphacidae).

b) Automictic pseudogamy. Known in Coleoptera (Anobiidae,

Curculionidae) and Lepidoptera (Psychidae).

2) Hybridogenesis (hemiclonal inheritance). Syngamy occurs and the

paternal genome is present and active in soma of offspring (all daughters) but
is eliminated during oogenesis. Known in Phasmatodea (Bacillidae) (26).

III. Mixed systems. Regular or irregular alternation between different genetic systems,
typically between amphimixis and thelytoky. Alternation between haploid-male and
diploid-male systems is unknown. There are many dimensions along with mixed systems
might be classified. The classification implicit in Figure 1 is as follows.

A) Thelytoky (or polyembryony) alternating with haplodiploidy.

1) Cyclic alternation.

a) Polyembryony. Clonal proliferation of embryos (male or female) by

fission. Found in Hymenoptera (Dryinidae, Braconidae, Platygasteridae,
Encyrtidae) (17).

2 of 6 11/11/2017, 5:45 PM
CLASSIFICATION OF THE MAJOR GENETIC SYSTEMS OF INSECTS http://www.annualreviews.org/doi/suppl/10.1146/annurev.ento.48.09180...

b) Cyclic haplodiploidy-thelytoky (cyclic parthenogenesis)(18).

i) Fixed (single-generation) cycling. A single generation of

amphimixis alternates with a single generation of thelytoky.
Found in Hymenoptera (Cynipidae)(35).

ii) Flexible (several- to many-generation) cycling.

Reproduction is typically thelytokous, but an environmental cue
can trigger a switch to amphimixis. Found in Coleoptera
(Micromalthidae) (32), and Diptera (Cecidomyiidae) (20).

2) Facultative haplodiploidy-thelytoky (facultative parthenogenesis). Any of

various systems in which reproduction may be either amphimictic or
thelytokous. In most of these systems, reproduction is typically amphimictic,
but unmated females may produce some viable offspring by thelytoky.
Widespread in Hymenoptera (3, 13, 15, 21, 28, 34, 37). Also known in a few
Hemiptera (10).

B) Thelytoky alternating with diplodiploidy

1) Cyclic dipldiploidy-thelytoky (cyclic parthenogenesis) (18). Found in

Hemiptera (Aphididae).

2) Facultative diplodiploidy-thelytoky (facultative parthenogenesis).

Widespread in Ephemeroptera (2, 11, 12), Orthoptera (16, 31, 33, 38),
Phasmatodea (24, 27), Mantodea, Blattaria (8), Isoptera (1), and Lepidoptera
(9, 14). Also known in a few Psocoptera (4) and Diptera (22).

1. Afzal M, Salihah Z. 1985. Sex ratio, occurrence of parthenogenesis, ovarian development and
oviposition behavior of the primary reproductives of Bifiditermes beesoni (Isoptera,
Kalotermitidae). Z. Angew. Entomol. 100: 132-46

2. Ball SL. 2001. Tychoparthenogenesis and mixed mating in natural populations of the mayfly
Stenonema femoratum. Heredity 87: 373-80

3. Bandara HMJ, Walter GH. 1993. Virgin production of female offspring in a usually
arrhenotokous wasp, Spalangia endius Walker (Hymenoptera: Pteromalidae). J. Aust. Entomol.
Soc. 32: 127-8

4. Betz BW. 1983. The biology of Trichadenotecnum alexandrae Sommerman (Psocoptera:

Psocidae). II. Duration of biparental and parthenogenetic reproductive abilities. J. Kansas.
Entomol. Soc. 56: 420-6

5. Beukeboom LW. 1995. Sex determination in Hymenoptera: a need for genetic and molecular
studies. Bioessays 17: 813-7

6. Bull JJ. 1983. Evolution of sex determining mechanisms. Menlo Park, California:
Benjamin/Cummings

3 of 6 11/11/2017, 5:45 PM
CLASSIFICATION OF THE MAJOR GENETIC SYSTEMS OF INSECTS http://www.annualreviews.org/doi/suppl/10.1146/annurev.ento.48.09180...

7. Cook JM. 1993. Sex determination in the hymenoptera: A reviews of models and evidence.
Heredity 71: 421-35

8. Corley LS, Blankenship JR, Moore AJ. 2001. Genetic variation and asexual reproduction in
the facultatively parthenogenetic cockroach Nauphoeta cinerea: Implications for the evolution of
sex. J. Evol. Biol. 14: 68-74

9. Du MP. 1999. Parthenogenesis in the green oak tortrix, Tortrix viridana L.

(Lepidoptera,Torticidae). Bull. Soc. Entomol. France 104: 85-90

10. Foldi I. 1990. Morphology of the larval instars and imago of the male of Eurhizocossus
brasiliensis (Hampel in Wille, 1922) (Homoptera, Coccoidea, Margarodidae). Nouvelle Revue
D'Entomologie 7: 405-18

11. Gibbs KE, Siebenmann M. 1996. Life history attributes of the rare mayfly Siphlonisca
aerodromia Needham (Ephemeroptera: Siphlonuridae). Journal of the North American
Benthological Society 15: 95-105

12. Glazaczow A. 1994. Mayflies (Ephemeroptera) from the rivers Gwda and Drawa (in the
Pomeranian Lake District of North West Poland) and from some waters of their river basins.
Polskie Pismo Entomologiczne 63: 213-57

13. Grasso DA, Wenseleers T, Mori A, Le MF, Billen J. 2000. Thelytokous worker reproduction
and lack of Wolbachia infection in the harvesting ant Messor capitatus. Ethology Ecology and
Evolution 12: 309-14

14. Gubanov EA. 1993. The role of fertilization chamber in activation of mulberry silkworm
eggs to spontaneous parthenogenesis. Ontogenez 24: 52-6

15. Guglielmino A, Virla EG. 1998. Postembryonic development of Gonatopus lunatus Klug
(Hymenoptera: Dryinidae: Gonatopodinae), with remarks on its biology. Annales de la Societe
Entomologique de France 34: 321-33

16. Guseva VS, Litvinova NF, Tereshina SV. 1989. Parthenogenesis as a form of adaptation in
Acrididae (Orthoptera) (based on the example of Chorthippus apricarius L.). Entomologicheskoe
Obozrenie 68: 501-7

17. Hardy ICW, Ode PJ, Strand MR. 1993. Factors Influencing Brood Sex Ratios In
Polyembryonic Hymenoptera. Oecologia 93: 343-8

18. Hebert PDN. 1987. Genotypic characteristics of cyclic parthenogens and their obligately
asexual derivatives. In The evolution of sex and its consequences, ed. SJ Stearns, pp. 175-95.
Basel: Birhuser Verlag

19. Herrick G, Seger J. 1999. Imprinting and paternal genome elimination in insects. In Genomic
imprinting: an interdisciplinary approach, ed. R Ohlsson, pp. 41-71. Berlin: Springer-Verlag

20. Hodin J, Riddiford LM. 2000. Parallel alterations in the timing of ovarian Ecdysone Receptor
and Ultraspiracle expression characterize the independent evolution of larval reproduction in two
species of gall midges (Diptera: Cecidomyiidae). Dev. Genes Evol. 210: 358-72

4 of 6 11/11/2017, 5:45 PM
CLASSIFICATION OF THE MAJOR GENETIC SYSTEMS OF INSECTS http://www.annualreviews.org/doi/suppl/10.1146/annurev.ento.48.09180...

21. Hlldobler B, Wilson EO. 1990. The ants. Cambridge, Massachusetts: Harvard University
Press

22. Kramer MG, Templeton AR. 2001. Life-history changes that accompany the transition from
sexual to parthenogenetic reproduction in Drosophila mercatorum. Evolution 55: 748-61.

23. Lamb RY, Willey RB. 1987. Cytological mechanism of thelytokous parthenogenesis in
insects. Genome 29: 367-9

24. Lau D. 1987. Propagation and mating behaviour of the Annan-phasmid Baculum
extradentatum (Brunner von Wattenwyl). Zoologischer Anzeiger 218: 81-92

25. Mable BK, Otto SP. 1998. The evolution of life cycles with haploid and diploid phases.
BioEssays 20: 453-62

26. Mantovani B, Scali V. 1992. Hybridogenesis and androgenesis in the stick-insect Bacillus
rossius-grandii benazzii (Insecta, Phasmatodea). Evolution 46: 783-96

27. Mantovani B, Tinti F, Barilani M, Scali V. 1996. Current reproductive isolation between
ancestors of natural hybrids in Bacillus stick insects (Insecta: Phasmatodea). Heredity 77: 261-8

28. Moritz RF, Haberl M. 1994. Lack of meiotic recombination in thelytokous parthenogenesis
of laying workers of Apis mellifera capensis (the Cape honeybee). Heredity 73: 98-102

29. Normark BB. 1999. Evolution in a putatively ancient asexual aphid lineage: recombination
and rapid karyotype change. Evolution 53: 1458-69

30. Nur U. 1980. Evolution of unusual chromosome systems in scale insects (Coccoidea:
Homoptera). In Insect Cytogenetics, ed. RL Blackman, GM Hewitt, M Ashburner, pp. 97-117.
London: Blackwell Scientific Publications

31. Pardo MC, Lopez Leon MD, Cabrero J, Camacho JPM. 1995. Cytological and
developmental analysis of tychoparthenogenesis in Locusta migratoria. Heredity 75: 485-94

32. Pollock DA, Normark BB. 2002. The life cycle of Micromalthus debilis LeConte
(Coleoptera: Archostemmata: Micromalthidae): historical review and evolutionary perspective.
Journal of Systematics and Evolutionary Research (In press)

33. Rentz DCF, John B. 1990. Studies in Australian Gryllacrididae: Taxonomy, biology, ecology
and cytology. Invertebrate Taxonomy 3: 1053-210

34. Schmied A, Fuehrer E. 1996. The importance of ichneumon-flies in damage areas of

Pristiphora abietina Christ. Zeitschrift fuer Pflanzenkrankheiten und Pflanzenschutz 103: 644-57

35. Stone GN, Schnrogge K, Atkinson RJ, Bellido D, Pujade-Villar J. 2002. The population
biology of oak gall wasps (Hymenoptera: Cynipidae). Annu. Rev. Entomol. 47: 633-68

36. Suomalainen E, Saura A, Lokki J. 1987. Cytology and evolution in parthenogenesis. Boca
Raton: CRC Press

37. Tsuji K, Yamauchi K. 1995. Production of females by parthenogenesis in the ant, Cerapachys

5 of 6 11/11/2017, 5:45 PM
CLASSIFICATION OF THE MAJOR GENETIC SYSTEMS OF INSECTS http://www.annualreviews.org/doi/suppl/10.1146/annurev.ento.48.09180...

biroi. Insectes Sociaux 42: 333-6

38. Walker MP, Lewis CJ, Whitman DW. 1999. Effects of males on the fecundity and fertility of
female Romalea microptera grasshoppers. Journal of Orthoptera Research: 277-83

6 of 6 11/11/2017, 5:45 PM