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Conflictual speciation: species formation via genomic conflict

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A remarkable suite of forms of genomic conflict has recently been implicated in speciation. We propose that these diverse roles of genomic conflict in speciation processes can be unified using the concept of ‘conflictual speciation’. Conflictual speciation centers on the evolution of reproductive isolation as a byproduct of antagonistic selection among genomic elements with divergent fitness interests. Intragenomic conflicts are expected to readily generate Dobzhansky–Muller incompatibilities, due to population-specific interactions between opposing elements, and thus they could be especially important in speciation. Moreover, selection from genomic conflicts should be relatively unrelenting across ecological and evolutionary time scales. We explain how intragenomic conflicts can promote, or sometimes constrain, speciation, and describe evidence relating conflicts to the evolution of reproductive isolation.

Section snippets

How does selection promote speciation?

Natural selection contributes to speciation by the well-studied process of ecological speciation (ES), whereby divergent ecological selective pressures drive reproductive isolation (RI) between populations occupying different environments 1, 2 (Figure 1). An important alternative to ES, mutation-order speciation, involves different and incompatible alleles arising by chance, and increasing in frequency, in different populations that are subject to similar ecological selective pressures 1, 3.

What is intragenomic conflict?

We define intragenomic conflict as antagonistic interactions between DNA sequences, or their products, within an individual. The ‘genome’ is considered as all genetic material that is inherited. Conflict can involve elements that directly distort their own transmission rate positively, by either preferentially reaching gametes, interfering with transmission of alternative alleles, or replicating disproportionately to the rest of the genome [11]. Such direct-distorting elements should increase

How can intragenomic conflicts contribute to speciation?

ES involves divergence between populations due to genetically-based interactions between competitors, predators and prey, hosts and parasites, or mutualists, or adaptation to different abiotic conditions. By contrast, CS by intragenomic conflict involves divergence between populations due to antagonistic interactions between opposing elements within a genome. Such interactions are expected to lead to genetic divergence, between populations, in pairs or larger sets of

How can intragenomic conflicts oppose speciation?

Genomic conflict need not always promote speciation. In fact, it might sometimes oppose or constrain the process [19]. A key scenario concerns population divergence with some degree of gene flow. Suppose that two selectively and universally (in both populations) advantageous driver alleles have arisen in two different populations. The alleles will move between populations via gene flow, and because one allele will almost always have at least a slightly higher selective advantage than others, a

What empirical evidence supports the hypothesis of CS?

An especially important challenge for studies of CS, compared to ES, is that the phenotypic expression of intragenomic conflict is commonly either highly episodic, and thus difficult to capture in progress, or invisible unless perturbed by hybridization, and thus difficult to discern without experimental analyses or studies of hybrid zones [8]. Despite these limitations, a primary motivation for formalizing the hypothesis of CS has been the rapidly-expanding list of cases where reproductive

What predictions and tests can be used to further evaluate CS?

CS and ES differ with regard to factors favoring, or disfavoring, the evolution of reproductive isolation (Table 2). These differences serve as bases for developing empirical tests of CS in relation to ES and other processes of speciation.

CS is driven by conflict at the genetic level. Thus, ideal tests of CS involve molecular-genetic information concerning the conflicting elements causing reproductive isolation. For example, a positive relationship is predicted between the degree of overall

Conclusions and future directions

We have presented a conceptual framework for understanding and analyzing how speciation can be driven by selection due to intragenomic conflict, a process intrinsic to every organism. A rapidly-increasing body of empirical evidence supports the importance of conflictual interactions in the evolution of reproductive isolation. However, few studies have conclusively linked intragenomic conflict with reproductive isolation, probably because such conflicts are difficult to demonstrate, and

Acknowledgments

We thank Francisco Úbeda, Steve Frank, Jeff Joy, Mikael Mökkönen, and the Simon Fraser University Fab-lab for helpful comments. We also thank Tom Price for discussions about meiotic drive, Sam Flaxman for points about the predictions of mutation-order speciation, Robert Trivers for discussions about conflict in general, and Aneil Agrawal for suggesting ‘anti-speciation’ effects of driving elements. P.N. is funded by the European Research Council (Starter Grant NatHisGen), and B.C. thanks NSERC

Glossary

Anti-speciation gene
a gene that constrains speciation by mediating increased gene flow and reduced reproductive isolation between populations.
Conflictual speciation
a mechanism of speciation whereby genomic conflicts drive the evolution of reproductive isolation.
Cytoplasmic male sterility
sterility of male function (pollen or sperm production or viability) caused by cytoplasmically-inherited elements, often mitochondria.
Dobzhansky–Muller incompatibilities
negatively-interacting sets of genes that

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