Abstract

Investigating fitness interactions in natural populations remains a considerable challenge. We take advantage of the unique population structure of Vibrio parahaemolyticus, a bacterial pathogen of humans and shrimp, to perform a genome-wide screen for coadapted genetic elements. We identified 90 interaction groups (IGs) involving 1,560 coding genes. 82 IGs are between accessory genes, many of which have functions related to carbohydrate transport and metabolism. Only 8 involve both core and accessory genomes. The largest includes 1,540 SNPs in 82 genes and 338 accessory genome elements, many involved in lateral flagella and cell wall biogenesis. The interactions have a complex hierarchical structure encoding at least four distinct ecological strategies. One strategy involves a divergent profile in multiple genome regions, while the others involve fewer genes and are more plastic. Our results imply that most genetic alliances are ephemeral but that increasingly complex strategies can evolve and eventually cause speciation.

Highlights

  • The importance of coadaptation to evolution was recognized by Darwin in the 6th edition of Origin of Species, where he wrote: ’In order that an animal should acquire some structure specially and largely developed, it is almost indispensable that several other parts should be modified and coadapted’ (Darwin, 1859)

  • The consequences of epistasis for the evolution of phenotypic diversity depends on transmission genetics, that is how genetic material is passed from one generation to the and population structure

  • The sample is subdivided into four distinct populations, which have different, currently overlapping, geographical distributions (Yang et al, 2019a). These four populations are clearly visible in Principle Coordination Analysis (PCoA) of the SNP variants in this dataset (Figure 1b)

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Summary

Introduction

The importance of coadaptation to evolution was recognized by Darwin in the 6th edition of Origin of Species, where he wrote: ’In order that an animal should acquire some structure specially and largely developed, it is almost indispensable that several other parts should be modified and coadapted’ (Darwin, 1859). Extensive linkage disequilibrium (LD) due to natural selection is rare (Pritchard and Przeworski, 2001) and it is difficult to maintain dissimilar genetic strategies concurrently in the same population unless the strategies are encoded by a small number of loci. This means that the coadaptation necessary for extensive phenotypic diversification can only take place when facilitated by barriers to gene flow, such as geographical separation, mate choice or the suppression of recombination for example by inversion polymorphisms (Dobzhansky, 1937; Wallace, 1991).

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