Genetic conflict, kin and the origins of novel genetic systems

Abstract

Genetic conflict may have played an important role in the evolution of novel genetic systems. The ancestral system of eumendelian genetics is highly symmetrical. Those derived from it (e.g. thelytokous parthenogenesis, haplodiploidy and parent-specific allele expression) are more asymmetrical in the genetic role played by maternal versus paternal alleles. These asymmetries may have arisen from maternal-paternal genetic conflict, or cytonuclear conflict, or from an interaction between them. Asymmetric genetic systems are much more common in terrestrial and freshwater taxa than in marine taxa. We suggest three reasons for this, based on the relative inhospitability of terrestrial environments to three types of organism: (i) pathogens-departure from the marine realm meant escape from many pathogens and parasites, reducing the need for sexual reproduction; (ii) symbionts-symbionts are no more important in the terrestrial realm than the marine realm but are more likely to be obligately intracellular and vertically transmitted, making them more likely to disrupt their host's genetic systems; (iii) Gametes and embryos-because neither gametes nor embryos can be shed into air as easily as into seawater, the mother's body is a more important environment for both types of organisms in the terrestrial realm than in the marine realm. This environment of asymmetric kinship (with neighbours more closely related by maternal alleles than by paternal alleles) may have helped to drive asymmetries in expression and transmission.

Keywords: Wolbachia; endosymbiont; genetic system; haplodiploidy; parthenogenesis.

Figure 1.

Asymmetric genetic systems, where the sperm and egg genome have different roles or fates [–11]. Each row of this figure describes a different asymmetric genetic system. The first column of each row shows the adult generation, the second column the gametes produced, the third column the embryos shortly after fertilization and the last column the offspring generation. The animal symbols represent males (in blue) and females (in red). Haploid individuals and gametes are shown with one chromosome. Diploid individuals and gametes are shown with two chromosomes. From top to bottom: Parthenogenesis = obligate thelytokous parthenogenesis, development of females from unfertilized eggs (including apomixis = egg production by mitosis and automixis = egg production involving meiosis). A few thousand eukaryote species, especially freshwater and terrestrial animals. Gynogenesis = development of females from fertilized eggs, but with only the mother's genome. Many groups including salamanders, fish, insects and angiosperms. Hybridogenesis = gynogenesis, except that the paternal genome is incorporated and expressed in the offspring but later eliminated from the offspring's germline. Several species of fish and frogs. Arrhenotoky = arrhenotokous haplodiploidy or haplodiploidy in the strict sense, development of males from unfertilized eggs. Males are haploid and never have a paternal genome at all. Several groups of insects and mites, oxyurid nematodes and monogonont rotifers. PGE = paternal genome elimination, development of males from fertilized eggs in which males have a paternal genome but do not transmit it. Males may lose their paternal genome either early in development, becoming haploid (early PGE) or retain their paternal genome without transmitting it (late PGE). A few groups of insects, mites and springtails. Androgenesis = development of either sex from fertilized eggs in which the sperm genome supplants egg genome. Offspring have the father's nuclear genome. A few clam species and Saharan cypress. Cyclic parthenogenesis = system in which one or more parthenogenetic generations regularly alternates with a sexual generation. Several groups including cladocera, monogonont rotifers, some loriciferans and several groups of insects.

Figure 2.

Adaptations of intracellular bacteria to increase their direct or indirect fitness by manipulating the reproduction of their host. Direct effects of endosymbiont (including reproductive manipulation and transmission) are indicated with solid arrows, while indirect effects that benefit related endosymbionts in different hosts are indicated with dashed arrows. Diploid individuals are represented by male or female symbols with two chromosomes. Haploid males are represented by a male symbol with one chromosome. The infection status of an individual is indicated by the presence of the red Wolbachia icon. (a) Feminization, conversion of males into females, here including feminization of parthenogenetically produced males (often referred to as ‘parthenogenesis-induction’; example Encarsia pergandiella, photo by Alex Wild), as well as feminization of sexually produced males (example Armadillidium vulgare, photo by Franco Folini). (b) Late male-killing, killing of males late in development, such that dead males can serve as a source of infection of nearby females (example Culex tarsalis, photo by Joseph Berger, Bugwood.org). (c) Early male-killing (EMK), killing of male embryos. When there is competition between host siblings, EMK enhances fitness of the bacterial clone inhabiting a single host individual (example Harmonia axyridis, photo by Alex Wild). (d) CI, modification of sperm to kill uninfected eggs. Infected eggs are rescued by an antitoxin. CI enhances the fitness of the bacterial clone(s) encoding compatible antitoxins (example Nasonia vitripennis, photo by Gernot Kunz).