Abstract
We look to mitonuclear ecology and the phenomenon of Mother’s Curse to argue that the sex of parents and offspring among populations of eukaryotic organisms, as well as the mitochondrial genome, ought to be taken into account in the conceptualization of evolutionary fitness. Subsequently, we show how characterizations of fitness considered by philosophers that do not take sex and the mitochondrial genome into account may suffer. Last, we reflect on the debate regarding the fundamentality of trait versus organism fitness and gesture at the idea that the former lies at the conceptual basis of evolutionary theory.
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Notes
As Grafen (2020, 9) notes, the possibility of alternative characterizations of fitness arises since, in Fisher’s fundamental theorem of natural selection, “the term fitness, which occurs as ‘mean fitness’ on the left-hand side of the fundamental theorem, and as ‘genetic variance of fitness’ on the right-hand side, is not actually defined by Fisher anywhere in his book or, indeed, elsewhere.” Furthermore, as discussed below, while Fisher already discussed important ideas in this paper, e.g., transgenerational aspects of fitness, we discuss fitness under current advancements in the field of mitonuclear ecology, which was not a field of study early in the twentieth century.
Eukaryotes are organisms whose cells contain membrane-bound organelles, among other traits that differ from prokaryotic organisms.
The F1 generation refers to the first filial generation.
There have been few exceptions to this phenomenon. See Luo et al. (2018).
Compare, for example, with Ariew and Ernst (2009, 290) two adequacy constraints: “(A) A fitness concept must be able to explain why one trait is expected to be better represented in a population under the influence of natural selection. … (B) A fitness concept must enable us to compare the degree to which natural selection will favor the spread of one trait over another, alternative trait.”
The vast majority of research into evolutionary theory has focused on the N genome of eukaryotic organisms, but eukaryotes also contain an entirely separate genome in the mitochondrion. The gene products of the mt genome regularly interact with gene products of the N genome.
Co-function of the mt and N genomes refers to the necessity of these two genomes to work together for oxidative phosphorylation (OXPHOS) to be carried out efficiently. This is due to the fact that some N genes that function in the mitochondrion must work alongside mt genes that also function in the mitochondrion; for example, genes that code for OXPHOS proteins of complexes in the electron transport system.
The eukaryotic cell was likely formed when an archaeon engulfed a bacterium approximately two billion years ago, where the archaeon genome became the N genome, and the bacterial genome became the mt genome. These genomes have been largely modified over the course of evolutionary history with the archaeon genome increasing to ~ 20,000 N genes, and the bacterial genome being reduced to 37 mt genes.
Here, propensity refers to a causal notion of probability, i.e., a “difference maker” or an aspect of a population that invokes change, as outline by Sober (2013).
Genetic hitchhiking occurs when deleterious alleles are inherited along with beneficial alleles since the mt genome does not recombine. As a result, the frequency of the deleterious alleles changes within a population based on selection of the beneficial alleles with which it is associated. If strong selection on one allele leads to the fixation of that allele plus all of the alleles with which it is associated, it is known as a selective sweep.
Of course, organisms do not truly have “goals” in the sense that they plan how many offspring they will produce and how long they will live. Here, the term “goal” refers to the fact that it is necessary for organisms to survive to reproductive age and reproduce in order to pass their genes to subsequent generations.
Quantitative genetics has certainly incorporated pedigrees and life history traits in models of selection (see Hadfield & Nakagawa, 2010), but here, we focus specifically on considerations of the mt genome and sex in conceptualizing fitness.
This will work differently if the mutation is on an N-mt gene (a N gene that functions in the mitochondrion), which can be passed down to offspring from both male and female parents. This will also be largely influenced by XY versus ZW mating systems.
N restorer genes are nuclear genes that evolve to counteract the detrimental effects of the mt genome. Such restorer genes seem to be rather widespread among eukaryotes.
As should be clear from our elaboration on this issue, we are not appealing to some special account of explanation, although causal, counterfactual, and/or probabilistic accounts of explanation could easily fit the bill. Our point is that on a basic and intuitive level of what is meant by explanation, taking sex and the mt genome into account is indispensable for a faithful representation of fitness in this scenario and an accurate understanding of the evolutionary forces at play in the discussed situation.
It is worthwhile to note that Pence and Ramsey (2015) do stress that TF1-TF3 are not equivalent and hint at some of the ideas that we develop here. For example, they note (1085): “If a trait has a significant benefit to individual organisms, yet is not (or not efficiently) transmitted from parents to offspring, then the TF3-fitness of that trait may be high while its TF2-fitness remains low.”.
See Sober (2013) on the importance of variation in trait fitness.
Perhaps it is worthwhile to add that, if our assessment in Sect. 5 is correct, and Abrams’ (2012) notion of parametric type fitness is one that takes essential components like sex and the mt genome into account, and if Abrams’ (2012) own argument to the effect that only parametric type fitnesses cause and explain evolution is correct, then there is another clear sense for which trait fitness is more fundamental than organism fitness (on the conceptual level). Namely, it is trait fitness that causes and explains evolution, not organism fitness.
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Acknowledgement
We wish to thank Marshall Abrams, Geoff Hill, Wendy Hood, Yoichi Ishida, Charles Pence, Matt Powers, Aaron Novick, and Matthew Wolak for helpful discussion and comments on an earlier draft of the paper
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Heine, K.B., Shech, E. Roles of mitonuclear ecology and sex in conceptualizing evolutionary fitness. Biol Philos 36, 29 (2021). https://doi.org/10.1007/s10539-021-09804-3
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DOI: https://doi.org/10.1007/s10539-021-09804-3