Mito-nuclear selection induces a trade-off between species ecological dominance and evolutionary lifespan

Micro-evolutionary processes acting in populations and communities ultimately produce macro-evolutionary patterns. However, current models of species life histories -- including processes of speciation, persistence, hybridization, and eventual extinction -- rarely connect these two time scales. This leaves us with a limited theoretical understanding of the subtleties of diversification, such as the relationship between species abundance in an ecological community and species longevity over evolutionary time, or the impact of selection on patterns of speciation and extinction when structuring an ecological community. Here we present a model for evolution in spatially extended populations with a focus on selection for mito-nuclear compatibility. We find that mito-nuclear selection acting at the individual level decreases genetic variability among species in a radiation, reducing the total number of species and skewing species abundances distributions towards mono-dominance. Also, intraspecific diversity increases as species become more abundant, leading to frequent evolutionary branching that reduces species lifetimes. The equilibrium of such communities is characterized by high rates of speciation, extinction, and hybridization, i.e., high turnover rate. These theoretical results are in concordance with empirical patterns of diversity across latitudinal gradients. Model predictions in the absence of mito-nuclear selection resemble the tropics, with high biodiversity, old species, and low speciation and extinction rates. Whereas model predictions under strong selection, which we expect in the harsh environments of temperate zones, produce fewer species and elevated recent speciation rates.

Nuclear selection is effectively policed by mating restrictions of the dikaryotic life cycle of mushroom-forming fungi

Altruistic social interactions generally evolve between genetically related individuals or other replicators, whereas sexual interactions usually occur among unrelated individuals. This tension between social and sexual interactions is resolved by policing mechanisms enforcing cooperation among genetically unrelated entities. For example, most organisms with two haploid genomes are diploid, both genomes encapsulated inside a single nuclear envelope. A fascinating exception to this are Basidiomycete fungi, where the two haploid genomes remain separate. Uniquely, the haploid nuclei of the dikaryon can fertilize subsequent gametes encountered, the presumed benefit of this lifecycle. The implications for the balance of selection within and among individuals are largely unexplored. We modelled the implications of a fitness tradeoff at the level of the haploid nucleus versus the level of the fungal individual. We show that the most important policing mechanism is prohibition of fusion between dikaryons, which can otherwise select for detrimental levels of nuclear mating fitness. An additional policing mechanism revealed by our model is linkage between loci with fitness consequences. Our results show that benefits of di-mon matings must be paired with policing mechanisms to avoid uncontrolled selection at the level of the nuclei. Furthermore, we discuss evolutionary implications of recent claims of nuclear exchange in related fungal groups.