The overall goal of the proposed research is to develop evolutionary genetic theory for understanding how co-transmission of host and microbial genomes affects co-evolution between hosts and their symbiotic or pathogenic microbes. Our approach is novel in that it extends theory of the inheritance of nuclear gene combinations within single genomes to gene combinations across two genomes, those of host and symbiont. Two-locus descent theory quantifies the coinheritance of gene combinations, whether in the same or in different genomes: the greater the coinheritance, the greater the degree to which the evolutionary trajectories of both genes are conjoined. Our results will allow us to interpret patterns of trans-genomic co- variation (interspecies disequilibria) in terms of th underlying causal evolutionary processes. We propose that coinheritance determines whether a host-symbiont association evolves toward enhanced virulence or toward benign mutualistic symbiosis. When applied to nuclear and mitochondrial gene combinations, we successfully predicted that the frequency of functional gene transfer from the mitochondria to the nucleus would be a function of the degree of selfing and discovered that inter-genomic transfer of functional genes is ten-fold more likely to occur in inbreeding species than in outcrossing species. Coinheritance of mitochondrial and nuclear genes in selfing mating systems allows selection to act more effectively on gene combinations than mating systems where nuclear and mitochondrial genes are inherited independently. Althoughmitochondria are wholly vertically transmitted like some symbionts, we expect similar effects to be manifest in systems with partial vertical transmission or in systems with contagious transmission of symbionts among host that are genetic relatives. In this proposed research we will address five specific aims which will develop theory to address the 1) generation and maintenance of interspecies disequilibria, 2) functional gene loss or transfer in host-symbiont associations, 3) coevolution of transmission mode, virulence, and population genetic structure. We propose to develop this more general theory, building upon progress from prior NIH funding.

Public Health Relevance

The overall goal of our proposed research is to develop a general evolutionary theory of the co- evolution and co-transmission of host and symbiont genomes. This is an important missing component of current investigations of the human micro-biome and its interpretation in regard to human health (Toft and Andersson 2011). In the context of human pathogens, we may better understand the conditions for disease emergence as well as those that favor increases and decreases in disease virulence (Anderson and May 1979;May and Anderson, 1979).

National Institute of Health (NIH)
National Institute of General Medical Sciences (NIGMS)
Research Project (R01)
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Genetic Variation and Evolution Study Section (GVE)
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Janes, Daniel E
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Indiana University Bloomington
Schools of Arts and Sciences
United States
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Drury, Douglas W; Dapper, Amy L; Siniard, Dylan J et al. (2017) CRISPR/Cas9 gene drives in genetically variable and nonrandomly mating wild populations. Sci Adv 3:e1601910
Dapper, Amy L; Wade, Michael J (2016) The evolution of sperm competition genes: The effect of mating system on levels of genetic variation within and between species. Evolution 70:502-11
Wolf, Jason B; Wade, Michael J (2016) Evolutionary genetics of maternal effects. Evolution 70:827-39
Ellen, Esther D; Peeters, Katrijn; Verhoeven, Merel et al. (2016) Direct and indirect genetic effects in life-history traits of flour beetles (Tribolium castaneum). Evolution 70:207-17
Wade, Michael J; Drown, Devin M (2016) Nuclear-mitochondrial epistasis: a gene's eye view of genomic conflict. Ecol Evol 6:6460-6472
Dapper, Amy L; Lively, Curtis M (2014) Interlocus sexually antagonistic coevolution can create indirect selection for increased recombination. Evolution 68:1216-24
Drown, Devin M; Wade, Michael J (2014) Runaway coevolution: adaptation to heritable and nonheritable environments. Evolution 68:3039-46
Wade, Michael J (2014) Paradox of mother's curse and the maternally provisioned offspring microbiome. Cold Spring Harb Perspect Biol 6:a017541
Drown, Devin M; Zee, Peter C; Brandvain, Yaniv et al. (2013) Evolution of transmission mode in obligate symbionts. Evol Ecol Res 15:43-59
Drown, Devin M; Dybdahl, Mark F; Gomulkiewicz, Richard (2013) Consumer-resource interactions and the evolution of migration. Evolution 67:3290-304

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