What Is Speciation? - PubMed (original) (raw)

Review

What Is Speciation?

B Jesse Shapiro et al. PLoS Genet. 2016.

Abstract

Concepts and definitions of species have been debated by generations of biologists and remain controversial. Microbes pose a particular challenge because of their genetic diversity, asexual reproduction, and often promiscuous horizontal gene transfer (HGT). However, microbes also present an opportunity to study and understand speciation because of their rapid evolution, both in nature and in the lab, and small, easily sequenced genomes. Here, we review how microbial population genomics has enabled us to catch speciation "in the act" and how the results have challenged and enriched our concepts of species, with implications for all domains of life. We describe how recombination (including HGT and introgression) has shaped the genomes of nascent microbial, animal, and plant species and argue for a prominent role of natural selection in initiating and maintaining speciation. We ask how universal is the process of speciation across the tree of life, and what lessons can be drawn from microbes? Comparative genomics showing the extent of HGT in natural populations certainly jeopardizes the relevance of vertical descent (i.e., the species tree) in speciation. Nevertheless, we conclude that species do indeed exist as clusters of genetic and ecological similarity and that speciation is driven primarily by natural selection, regardless of the balance between horizontal and vertical descent.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1

Fig 1. Units of species and speciation.

The Neo-Darwinian view of the Modern Synthesis is that "speciation genes" are the units driving speciation across the genome. Alternatively, if gene sets (including consortia of genes like plasmids or other mobile genetic elements) are sufficiently decoupled from their host genomes, this will lead to "gene ecology," in which gene sets, not species, determine reproductive isolation and/or adapt to ecological niches. Speciation could also be maintained (or potentially driven) by microbial symbionts or by host genes that select for particular symbionts, resulting in hologenome species. All of these speciation mechanisms can potentially be driven by selection or drift, and the list of units and mechanisms (arrows) is not exhaustive.

Fig 2

Fig 2. Models of speciation under different regimes of selection and recombination.

In all models, a single population of chromosomes (circles) splits into two nascent species, distinguishable by sets of genetic differences. At each time point, the most frequent multilocus genotype is shown, but other chromosomes could be segregating in the population at lower frequencies. Different haplotypes (or clonal frames) are shown as black or white circles. The ancestral niche is shown in blue and a new niche in orange. Gene flow (recombination) between species is indicated by horizontal connections between branches. (A) In the simplest model of speciation with gene flow, a single mutation controlling sexual isolation (but not under selection) is the only divergent locus (yellow square), with other loci experiencing gene flow between incipient species. (B) Selection during speciation can produce a pattern of genetic diversity across the genome very similar to (A), but species are expected to be longer-lived. Mutations under selection at early and later stages of speciation are shown as orange stars. (C) Allopatric speciation with a population bottleneck and neutral divergence of species. As in (A), competitive exclusion should lead to the extinction of one species if they come back into contact. (D) Without gene flow, the mutation under selection between species (orange star) will purge diversity genome-wide as it sweeps through one population, resulting in genome-wide divergence from the other population.

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References

    1. Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B. How Many Species Are There on Earth and in the Ocean? PLoS Biol. 2011;9: e1001127 10.1371/journal.pbio.1001127.s004 - DOI - PMC - PubMed
    1. Darwin C. The Origin of Species. London: John Murray; 1859.
    1. Mallet J. Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philos Trans R Soc Lond, B, Biol Sci. 2008;363: 2971–2986. 10.1073/pnas.92.7.2519 - DOI - PMC - PubMed
    1. Wu C-I. The genic view of the process of speciation. J Evol Biol. 2001;14: 851–865.
    1. Shapiro BJ, Polz MF. Ordering microbial diversity into ecologically and genetically cohesive units. Trends Microbiol. 2014;22: 235–247. 10.1016/j.tim.2014.02.006 - DOI - PMC - PubMed

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BJS was supported by a Canada Research Chair. The funders had no role in the preparation of the article.

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