What Microbial Population Genomics Has Taught Us About Speciation

Abstract

Population genomics has emerged as a valuable tool to define and delimit species and to understand the mechanisms that drive and maintain speciation. Species and speciation have been notoriously difficult to study in microbes owing to their asexual reproduction, promiscuous horizontal gene transfer, and obscure microscopic niches. Over the past few years, whole-genome sequencing of closely related, locally co-occurring populations of microbes, combined with simulations and modelling, has revealed certain general features of microbial speciation: it is usually driven by divergent natural selection between distinct ecological niches (a form of the ecological species concept), and species distinctness is maintained by barriers to gene flow (a form of the biological species concept). In some cases, gene-flow barriers may come about as a natural consequence of ecological specialization. Although these features appear to be quite general, there are exceptions. Trivially, barriers to gene flow cannot be used to delimit clonal populations where there is negligible gene flow. More interestingly, it is unclear whether other barriers to gene flow, such as genetic incompatibilities or differences in phage-host range, are able to drive speciation in the absence of other selective pressures. Here, I discuss the extent to which speciation is driven by natural selection, gene-flow barriers, or a combination of the two, drawing on recent examples from bacterial and archaeal population genomics, experimental evolution, and modelling. I then describe how population genomic data can be used to define and delimit species boundaries, based upon nucleotide identity cutoffs or upon discontinuities in gene flow. Despite important limitations and caveats, delimitation methods provide a useful starting point for more detailed investigation into the genetic and ecological basis of speciation.

Glossary

Niche

A specific set of ecological parameters (environments, resources, physical and chemical characteristics, biotic interactions, etc.) to which an organism is adapted. This does not necessarily imply (but does not exclude) physical separation between niches. For the purposes of this chapter, “niche” and “habitat” are used more or less interchangeably, although “habitat” has a more spatial connotation, while niches can be temporal, behavioural, physiological, etc.

Ecological species concept (ESC)

A species concept in which speciation is driven by adaptation to distinct habitats or ecological niches, with each species inhabiting a distinct niche.

Biological species concept (BSC)

A species concept based on reproductive isolation (in the strict sense) or to barriers to gene flow, resulting in more gene flow within than between species, even if some between-species gene flow still occurs.

Allopatric speciation

Speciation driven by physical barriers to gene flow between incipient species, such that speciation may occur in the absence of natural selection.

Sympatric speciation

Speciation that occurs in the absence of physical barriers to gene flow, such that speciation must be driven by some combination of natural selection and/or genetic barriers to gene flow.

Mosaic sympatry

An intermediate between sympatry and allopatric, in which organisms inhabit different niches (e.g. particles or hosts) within an otherwise well-mixed environment.

Gene flow

A general term for exchange of DNA between chromosomes, including both homologous and nonhomologous DNA. In sexual organisms, gene flow occurs during meiosis. In microbes, gene flow can occur by phage-mediated transduction, plasmid-mediated conjugation, or natural competence (uptake of free DNA) followed by homologous or nonhomologous recombination.

Gene-specific selective sweep

The process in which an adaptive gene or allele spreads in a population by recombination faster than by clonal expansion. The result is that the adaptive variant is present in more than a single clonal background and that diversity is not purged genome-wide.

Genome-wide selective sweep

The process in which an adaptive gene or allele spreads in a population by clonal expansion of the genome that first acquired it. The result is that diversity is purged genome-wide and that the adaptive variant is linked in the same clonal frame as the rest of the genome.

ecoSNP

An ecologically associated single nucleotide polymorphism (SNP) with different nucleotides fixed between two different habitats (e.g. an A allele in habitat 1 and a T allele in habitat 2). Genes under divergent natural selection between niches or habitats (“niche-specifying genes”) are expected to contain a large number of ecoSNPs.