Reversing mother's curse: selection on male mitochondrial fitness effects

Michael J Wade1, Yaniv Brandvain

  • 1Department of Biology, Indiana University, Bloomington, Indiana, 47405, USA. mjwade@indiana.edu

Insights

Mitochondria can evolve to affect male traits despite only being inherited maternally. Inbreeding and kin selection enable mitochondria to impact male fertility and viability, challenging previous assumptions.

Area of Science:

  • Evolutionary Biology
  • Genetics
  • Cell Biology

Background:

  • Organelles and endosymbionts, like mitochondria, are typically inherited maternally.
  • This maternal inheritance was thought to prevent selection on traits affecting male viability and fertility.

Purpose of the Study:

  • To investigate mechanisms allowing mitochondria to be selected for effects on male viability and fertility.
  • To challenge the dogma that paternal transmission is required for such selection.

Main Methods:

  • Theoretical modeling exploring the effects of inbreeding and kin selection.
  • Analysis of how these mechanisms associate mitochondrial traits with male fitness.

Main Results:

  • Inbreeding allows selection on male fertility traits by linking them to mitochondrial lineages.
  • Kin selection enables selection on male viability traits through indirect fitness benefits to sisters.
  • Conditions exist where harmful-to-female mitochondrial traits can spread.

Conclusions:

  • Mitochondrial evolution is not solely constrained by maternal inheritance.
  • Inbreeding and kin selection are key evolutionary forces shaping mitochondrial genomes.
  • These findings have implications for understanding organelle evolution, genomic conflict, and the evolution of harmful traits.

Related Concept Videos

Animal Mitochondrial Genetics02:59

Animal Mitochondrial Genetics

Among all the organelles in an animal cell, only mitochondria have their own independent genomes. Animal mitochondrial DNA is a double-stranded, closed-circular molecule with around 20,000 base pairs. Mitochondrial DNA is unique in that one of its two strands, the heavy, or H, -strand is guanine rich, whereas the complementary strand is cytosine rich and called the light, or L, -strand. Compared to nuclear DNA, mitochondrial DNA has a very low percentage of non-coding regions and is marked by...
Meiosis I03:09

Meiosis I

Meiosis is the division of a diploid cell into haploid cells forming sperm and eggs in animals through differentiation. Meiosis I is the first stage of meiosis, where the genetic recombination of homologous chromosomes and the reduction of the ploidy level by half occurs.
Prophase I is the most extended and complex step of meiosis I characterized by synapsis, chromosome pairing, and recombination of the homologous chromosomes. This process is facilitated by a proteinaceous structure called the...
X-linked Traits01:19

X-linked Traits

In most mammalian species, females have two X sex chromosomes and males have an X and Y. As a result, mutations on the X chromosome in females may be masked by the presence of a normal allele on the second X. In contrast, a mutation on the X chromosome in males more often causes observable biological defects, as there is no normal X to compensate. Trait variations arising from mutations on the X chromosome are called “X-linked”.
Frequency-dependent Selection01:21

Frequency-dependent Selection

When the fitness of a trait is influenced by how common it is (i.e., its frequency) relative to different traits within a population, this is referred to as frequency-dependent selection. Frequency-dependent selection may occur between species or within a single species. This type of selection can either be positive—with more common phenotypes having higher fitness—or negative, with rarer phenotypes conferring increased fitness.Positive Frequency-Dependent SelectionIn positive...
Mismatch Repair01:20

Mismatch Repair

Organisms are capable of detecting and fixing nucleotide mismatches that occur during DNA replication. This sophisticated process requires identifying the new strand and replacing the erroneous bases with correct nucleotides. Mismatch repair is coordinated by many proteins in both prokaryotes and eukaryotes.
The Mutator Protein Family Plays a Key Role in DNA Mismatch Repair
The human genome has more than 3 billion base pairs of DNA per cell. Prior to cell division, that vast amount of genetic...
Nondisjunction01:21

Nondisjunction

Nondisjunction is the failure of homologous chromosomes or sister chromatids to separate correctly and move to the opposite poles of the cells. This produces daughter cells with abnormal chromosome numbers.  Nondisjunction is common during anaphase I or anaphase II of meiosis.  Mutations in synaptonemal complex proteins that attach homologous chromosomes increase the chances of nondisjunction in anaphase I of meiosis I. In contrast, mutations in topoisomerases and condensins that hold sister...