Maternal transmission, sex ratio distortion, and mitochondria

Abstract

In virtually all multicellular eukaryotes, mitochondria are transmitted exclusively through one parent, usually the mother. In this short review, we discuss some of the major consequences of uniparental transmission of mitochondria, including deleterious effects in males and selection for increased transmission through females. Many of these consequences, particularly sex ratio distortion, have well-studied parallels in other maternally transmitted genetic elements, such as bacterial endosymbionts of arthropods. We also discuss the consequences of linkage between mitochondria and other maternally transmitted genetic elements, including the role of cytonuclear incompatibilities in maintaining polymorphism. Finally, as a case study, we discuss a recently discovered maternally transmitted sex ratio distortion in an insect that is associated with extraordinarily divergent mitochondria.

Keywords: Wolbachia; cytoplasmic male sterility; genetic conflict; reproductive parasitism; symbiosis.

Fig. 1.

Three possible consequences of maternal transmission of mitochondria (and other maternally transmitted organelles and symbionts). (A) Mutations that are deleterious in males can become common if they do not decrease female fitness. (B) Maternally transmitted lineages that increase the frequency of females will be favored by selection. (C) Mitochondria and maternally transmitted symbionts are linked, such that symbionts that spread in a population will bring their associated mitochondrial haplotype along with them. Different colors represent different haplotypes. Mt, mitochondria; S, symbiont.

Fig. 2.

Distorter (A) and normal (B) L. nr. bostrychophila have radically different mitochondrial genome order and organization. Protein-coding and ribosomal genes are labeled; genes on the forward/complementary strand are on the outside/inside of the circles. Similarity between genes ranges from 53–80%: ATP6 (75.4%), ATP8 (65.4%), CO1 (76.6%), CO2 (73.9%), CO3 (70.6%), COB (76.8%), ND1 (76.1%), ND2 (73.8%), ND3 (76.8%), ND4 (72.4%), ND4L (75.9%), ND5 (70.9%), ND6 (53.1%), 12S (80.1%), 16S (80.1%). Although all circles have been closed using PCR, a few have not been completely sequenced, and these are indicated by the small gaps. Normal minicircle sizes (minicircles are named for their largest gene): 16S (3,265 bp), ND4 (3,426 bp), CO1 (3,147 bp), ATP6 (2,714 bp), ND6 (1,354 bp), ND1 (1,275 bp), ND5 (>3,717 bp). Distorter minicircle sizes: 16S (2,746 bp), ND4 (5,312 bp), CO1 (5,626 bp), 12S (2,131 bp), ND5 (∼4,600 bp).

Fig. 3.

Distinctive mitochondrial morphology in rectal glands of distorter females. (A) TEM of 4-wk-old normal female rectal gland, showing mitochondria with intact cristae, many intact scalariform junctions (i.e., parallel plasma membranes), and even ground substance (i.e., cytosol) between the two. (B) Close-up of previous image. (C) TEM of 4-wk-old distorter female rectal gland, showing abnormal mitochondria with fragmented, electron dense material within and few cristae, few intact scalariform junctions, and condensed ground substance between the two. (D) Close-up of previous image. (E and F) Light micrograph of sagittal section of a normal female with arrows to indicate the location of the glands. (Scale bars: 500 nm in A–D and 50 μm in E and F.)

Fig. 4.

Distorter L. nr. bostrychophila females have a significantly shorter lifespan than normal females (coxph: df = 1, P < 0.001; n = 51 and 32 for distorter and normal females, respectively). Crosses indicate censored data (two individuals were lost during the experiment and one individual survived past the end of the experiment).