Role of Natural Selection in Chromosomal Speciation


Speciation can occur in the face of gene flow if there are mechanisms that are able to neutralise it. Two such mechanisms or forces are divergent selection and the suppression of recombination. New data and theory suggest that chromosomal rearrangements (CRs) facilitate speciation with gene flow mainly by suppressing recombination. However, the role of natural selection in chromosomal speciation is less clear. According to recent models, natural selection can play a role in speciation by facilitating the fixation of CRs; and later, acting synergistically with CRs, by allowing the accumulation of incompatibilities along large regions of the genome. Interestingly, instead of resulting exclusively from disruptive selection among populations, a potential signal of selection within CRs may also result from the inability of favourable mutations to migrate between populations. However, empirical evidence for natural selection in suppressedā€recombination chromosomal speciation is scarce, reinforcing the need for further multidisciplinary studies.

Key Concepts:

  • For evolutionary biologists, speciation has always been a controversial topic, both in terms of mechanisms and geographical context.

  • Although allopatry has been the most consensual geographic context of speciation, the divergence of taxa in the face of gene flow is not a rare observation.

  • In purely genetic terms, speciation can be viewed as the evolution of restrictions on the freedom of genetic recombination.

  • Recombination originates new genetic combinations upon which natural selection can act, transforming the genomes of lineages connected by gene flow into a mosaic of genetic information.

  • The molecular characterisation of genes involved in reproductive isolation between some Drosophila species suggests that natural selection has shaped their evolution.

  • The functional characterisation of genes involved in reproductive isolation suggests that genetic conflicts may have a more important role in speciation than what it was initially thought.

  • The formalisation of suppressedā€recombination models of speciation was highly influenced by research performed in fruit flies and sunflowers (Drosophila and Helianthus).

  • CRs may play an important role in the origin and accumulation of incompatibilities between parapatric populations but also by avoiding species fusion after a secondary contact.

  • Signatures of selection within CRs may result from divergent environmental conditions but also from universally advantageous alleles.

  • Although, in theory, natural selection facilitates the role of CRs in speciation, signatures of natural selection within CRs have not been universally found in the species so far investigated.

Keywords: chromosomal rearrangements; natural selection; gene flow; recombination; reproductive isolation; breakpoints; genetic conflict; gene movement; genomic neighbourhood; reinforcement

Figure 1.

Recombination as a source of genetic diversity. In the absence of recombination (a), F1 hybrids produce only two types of gametes for a given chromosome pair, the same as their parents. In this case, phenotypic diversity is basically generated by mutation and random segregation of the different pairs of chromosomes. In scenario (b), recombination during the F1s meiosis shuffles genetic material, generating multiple genetic combinations of the information received from parents, which results in additional phenotypic diversity upon which natural selection can act.

Figure 2.

The Navarro–Barton model of chromosomal speciation. (Figure from: Faria and Navarro, ). Reproduced with permission of Elsevier. The Navarro–Barton model (Navarro and Barton, ) was conceived to test the efficiency of CRs in delaying gene flow of alleles that are advantageous under the environmental conditions of the two populations. For contrasting purposes two scenarios are presented: (i) no initial fixed CRs differences between populations (a1); and (ii) at least one fixed CRs difference between populations (a2). An advantageous mutation that occurs in collinear regions in any population (black asterisk) will spread, first within their population of origin and, afterwards, all over the species range (b1), unless it is trapped by an inversion and cannot easily recombine (b2). Under these circumstances, its spread to the other population will be delayed relative to alleles outside the rearrangement or relative to alleles from other chromosomes without CRs (b2). The delay in the spread of the black mutation into population 1 can be enough for new mutations to occur in the region encompassed by the CR (red square – c2) that may be incompatible with the black allele. If this is the case, this advantageous red mutation will become fixed in population 1, but when it arrives at the hybrid zone, where it meets for the first time an incompatible allele (black asterisk), it will not be able to spread into population 2 (c2). In contrast, in scenario c1, the black asterisk mutation will spread from population 2 to population 1 and get fixed in both populations. Thus, when the red square mutation appears in population 1, it will be immediately eliminated (red cross) because it is incompatible with the black allele. Other advantageous alleles that subsequently appear (white square – c1 and c2), which may or not be involved in incompatibilities with existing alleles, will spread and get fixed in both populations (d1), or will only get fixed within its population of origin if trapped within a CR (d2). The probability that new incompatible alleles will arise and get established will keep increasing, triggering the so called ‘snowball effect’.

Figure 3.

Fixation of CRs: the Kirkpatrick–Barton model. (Figure from Faria and Navarro, ). Reproduced with permission of Elsevier. The model proposed by Kirkpatrick and Barton (Kirkpatrick and Barton, ) explains how, under divergent selection, alternative CRs can get fixed in two recently diverged parapatric populations (a). Overtime (b), mutations occur at a minimum of two loci in population 1 (green asterisks) that are favourable under local environmental conditions but that are disadvantageous in population 2. According to the authors, the two loci are not tightly linked, otherwise they would work as a single gene and the model would not apply. The two alleles will spread and get fixed only within population 1. During this period, a neutral or weakly underdominant CR (e.g. pericentric inversion, in yellow) occurs within population 2 (b) that confers similar fitness as the collinear chromosomes in that same population. However, in contrast to collinear chromosomes, the rearranged region will recombine less (or not at all) with chromosomes arriving from population 1 and, therefore, the alleles that the inversion carry never suffer the ‘Achilles’ heel’ of being found on the same chromosome with the ‘immigrant’ disadvantageous alleles at the other locus. The rearranged chromosomes will thus carry a combination of alleles at two loci that present higher fitness in the environmental conditions of population 2 than the recombining chromosomes (r), which tend to be eliminated (red cross). The chromosome with the inversions will therefore increase in frequency (c) resulting in two populations with a set of alleles that are locally adapted and with almost fixed alternative arrangements (d).

Figure 4.

Visual metaphor of genomic islands of divergence. (Figure from: Nosil et al., ). Reproduced with permission of John Wiley and Sons. Schematic illustration comparing the expected patterns of genomic differentiation between models with versus without gene flow. IBA, isolation by adaptation. According to Nosil and collaborators (2009), islands of divergence are genomic regions exhibiting greater differentiation than expected under neutrality, thereby rising above sea level (neutrality threshold): ‘…an island is composed of loci – both selected (dark grey) and tightly linked neutral (white) loci – that should be identifiable as outliers in a genome scan. Loosely linked (light grey) loci are depicted as regions far enough from selected loci to fall below sea level as non outliers, but still close to the surface, being more differentiated than most unlinked neutral loci’. Selection contributes both to island elevation (differentiation) and island size (contiguous highly differentiated loci), and the origin and growth of genomic islands may be facilitated by the structural organisation of the genome (structural model), particularly by CRs (Nosil et al., ). Reproduced with permission from Nosil et al. .



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Faria, Rui, Neto, Sandra, Noor, Mohamed AF, and Navarro, Arcadi(May 2011) Role of Natural Selection in Chromosomal Speciation. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0022850]