Mating ecology explains patterns of genome elimination

Abstract

Genome elimination - whereby an individual discards chromosomes inherited from one parent, and transmits only those inherited from the other parent - is found across thousands of animal species. It is more common in association with inbreeding, under male heterogamety, in males, and in the form of paternal genome elimination. However, the reasons for this broad pattern remain unclear. We develop a mathematical model to determine how degree of inbreeding, sex determination, genomic location, pattern of gene expression and parental origin of the eliminated genome interact to determine the fate of genome-elimination alleles. We find that: inbreeding promotes paternal genome elimination in the heterogametic sex; this may incur population extinction under female heterogamety, owing to eradication of males; and extinction is averted under male heterogamety, owing to countervailing sex-ratio selection. Thus, we explain the observed pattern of genome elimination. Our results highlight the interaction between mating system, sex-ratio selection and intragenomic conflict.

Keywords: Extinction; genomic imprinting; haplodiploidy; inbreeding; meiotic drive; paternal genome elimination; paternal genome loss; sex determination; sex ratio; sib-mating.

Figure 1

Parent-of-origin-specific genome elimination (GE), whereby an individual discards the chromosomes inherited from one parent, and transmits only those inherited from the other parent. We include only those cases where GE is sex-limited. Rows represent independent origins of GE. Column 1: adult generation. Column 2: gametes produced. Column 3: embryos shortly after fertilisation. Column 4: offspring soma. Column 5: offspring germline. Blue: male. Red: female. X: presence of X-chromosome (colour indicates parental origin). L in fungus-gnat entry: a germline-linked chromosome. Blue circle in mealybugs and coffee-borer-beetles entries: complete heterochromatisation of paternal genome. ‘?’ in body-louse entry: lack of information about somatic effects. ‘Germline PGE’: eliminated genome retained throughout development but not transmitted to offspring. ‘Embryonic PGE’: eliminated genome lost early in development, resulting in haploidy.

Figure 2

The consequences of genome elimination (GE) for offspring sex ratio. GE in the homogametic sex – that is, females under XX or XO sex determination (panels a & c) and males under ZW or ZO sex determination (panels f & h) – has no impact on offspring sex ratio. Paternal genome elimination (PGE) in the heterogametic sex – that is, males under XX or XO sex determination (panel b) and females under ZW or ZO sex determination (panel e) – leads to a female-biased offspring sex ratio. Maternal genome elimination (MGE) in the heterogametic sex – that is, males under XX or XO sex determination (panel d) and females under ZW or ZO sex determination (panel g) – leads to a male-biased offspring sex ratio.

Figure 3

The origin of genome elimination (GE). Results of the invasion analyses, for: (a) Paternal genome elimination (PGE) in females under XY or XO sex determination; (b) PGE in males, XY/XO; (c) Maternal genome elimination (MGE) in females, XY/XO; (d) MGE in males, XY/XO; (e) PGE in females, ZW/ZO; (f) PGE in males, ZW/ZO; (g) MGE in females, ZW/ZO; (h) MGE in males, ZW/ZO. In each case, potential for GE is shown for each class of genic actor, for whole-range of sib-mating (0 ≤  a ≤ 1). A: autosomal gene. X: X-linked gene. Y: Y-linked gene. Z: Z-linked gene. W: W-linked gene. Unimprinted autosomal genes (black lines) have positive potential for GE only under sib-mating (a > 0), and for PGE in heterogametic males (panel b) or PGE in heterogametic females (panel e), and so these are the scenarios in which GE robustly invades.

Figure 4

The maintenance of genome elimination (GE). Results of the evolutionary equilibrium analyses, for: (a) Paternal genome elimination (PGE) in heterogametic males (i.e. XY or XO sex determination); and (b) PGE in heterogametic females (i.e. ZW or ZO sex determination). In each case, the equilibrium level of PGE is shown for each class of genic actor, over the whole-range of sib-mating (0 ≤ a ≤ 1). A indicates an autosomal gene, X indicates an X-linked gene, Y indicates a Y-linked gene, Z indicates a Z-linked gene and W indicates a W-linked gene. Unimprinted autosomal genes (black lines) favour an intermediate level of PGE under male heterogamety (panel a), owing to countervailing sex-ratio selection, and fixation of PGE – leading to population extinction – under female heterogamety (panel b), owing to a lack of countervailing sex-ratio selection, so PGE in heterogametic males is the only scenario in which the population robustly survives the evolution of GE.