Dynamics of mitochondrial inheritance in the evolution of binary mating types and two sexes

Abstract

The uniparental inheritance (UPI) of mitochondria is thought to explain the evolution of two mating types or even true sexes with anisogametes. However, the exact role of UPI is not clearly understood. Here, we develop a new model, which considers the spread of UPI mutants within a biparental inheritance (BPI) population. Our model explicitly considers mitochondrial mutation and selection in parallel with the spread of UPI mutants and self-incompatible mating types. In line with earlier work, we find that UPI improves fitness under mitochondrial mutation accumulation, selfish conflict and mitonuclear coadaptation. However, we find that as UPI increases in the population its relative fitness advantage diminishes in a frequency-dependent manner. The fitness benefits of UPI ‘leak’ into the biparentally reproducing part of the population through successive matings, limiting the spread of UPI. Critically, while this process favours some degree of UPI, it neither leads to the establishment of linked mating types nor the collapse of multiple mating types to two. Only when two mating types exist beforehand can associated UPI mutants spread to fixation under the pressure of high mitochondrial mutation rate, large mitochondrial population size and selfish mutants. Variation in these parameters could account for the range of UPI actually observed in nature, from strict UPI in some Chlamydomonas species to BPI in yeast. We conclude that UPI of mitochondria alone is unlikely to have driven the evolution of two mating types in unicellular eukaryotes.

Origins of Eukaryotic Sexual Reproduction

“…Hadjivasiliou et al (2013) present arguments against this hypothesis, concluding that mating-type systems would have been buttressed but are not likely to have been initiated by uniparental systems.…”

“…A number of theoretical studies, cited in Hadjivasiliou et al (2013), have posited that the uniparental inheritance of organelles, considered in a later section of this review, preceded, and led to, the instantiation of mating types. Hadjivasiliou et al (2013) present arguments against this hypothesis, concluding that mating-type systems would have been buttressed but are not likely to have been initiated by uniparental systems.…”

Bioenergetic Constraints on the Evolution of Complex Life

“…Different zygotes then have different clones of mitochondria, increasing the variance across the population. This facilitates selection for the best mitochondria, at the level of the host cell, in much the same way as sex (Hadjivasiliou et al 2012(Hadjivasiliou et al , 2013. In contrast, biparental inheritance of mitochondria decreases variance between zygotes and interferes with selection (Hadjivasiliou et al 2012(Hadjivasiliou et al , 2013.…”

“…This facilitates selection for the best mitochondria, at the level of the host cell, in much the same way as sex (Hadjivasiliou et al 2012(Hadjivasiliou et al , 2013. In contrast, biparental inheritance of mitochondria decreases variance between zygotes and interferes with selection (Hadjivasiliou et al 2012(Hadjivasiliou et al , 2013. This is one of the deepest distinctions between the two sexes, even in isogametic algae and fungi: One sex passes on mitochondria, and the other does not (Hurst and Hamilton 1992).…”

Regular bottlenecks and restrictions to somatic fusion prevent the accumulation of mitochondrial defects inNeurospora

“…preventing 'infection' of other lineages [6][7][8]. Furthermore, an mtDNA bottleneck during egg cell formation has been shown in mice [9][10][11], redistributing mtDNA variation from within cells to among cells, and facilitating selection among individuals [12], as well as purifying selection in the germline [13].…”