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Abstract When gene flow accompanies speciation, recombination can decouple divergently selected loci and loci conferring reproductive isolation. This barrier to sympatric divergence disappears when assortative mating and disruptive selection involve the same “magic” trait. Although magic traits could be widespread, the relative importance of different types of magic traits to speciation remains unclear. Because body size frequently contributes to host adaptation and assortative mating in plant-feeding insects, we evaluated several magic trait predictions for this trait in a pair of sympatric Neodiprion sawfly species adapted to different pine hosts. A large morphological dataset revealed that sawfly adults from populations and species that use thicker-needled pines are consistently larger than those that use thinner-needled pines. Fitness data from recombinant backcross females revealed that egg size is under divergent selection between the preferred pines. Lastly, mating assays revealed strong size-assortative mating within and between species in three different crosses, with the strongest prezygotic isolation between populations that have the greatest interspecific size differences. Together, our data support body size as a magic trait in pine sawflies and possibly many other plant-feeding insects. Our work also demonstrates how intraspecific variation in morphology and ecology can cause geographic variation in the strength of prezygotic isolation.
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Reproductive isolation is a heuristic, not a measure: a commentary on Westram et al., 2022
Abstract Reproductive isolation is the heuristic basis of the biological species concept, but what is it? Westram et al. (this issue) propose that it is a measurable quantity, “barrier strength,” that prevents gene flow among populations. However, their attempt to make the concept of reproductive isolation more scientific is unlikely to satisfy the diverse opinions of all evolutionary biologists. There are many different opinions about the nature of species, even under the biological species concept. Complete reproductive isolation, where gene flow is effectively zero, is regarded by some biologists as an important end point of speciation. Others, including Westram et al., argue for a more nuanced approach, and they also suggest that reproductive isolation may differ in different parts of the genome due to variation in genetic linkage to divergently selected loci. In contrast to both these approaches, we favour as a key criterion of speciation the stable coexistence of divergent populations in sympatry. Obviously, such populations must be reproductively isolated in some sense, but neither the fraction of the genome that is exchanged, nor measures of overall barrier strength acting on neutral variation will yield very precise predictions as to species status. Although an overall measure of reproductive isolation is virtually unattainable for these reasons, its early generation components, such as assortative mating, divergent selection, or hybrid inviability and sterility are readily measurable and remain informative. For example, we can make the prediction that to remain divergent in sympatry, almost all sexual species will require strong assortative mating, as well as some sort of ecological or intrinsic selection against hybrids and introgressed variants.
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- Award ID(s):
- 2021181
- PAR ID:
- 10465710
- Date Published:
- Journal Name:
- Journal of Evolutionary Biology
- Volume:
- 35
- Issue:
- 9
- ISSN:
- 1010-061X
- Page Range / eLocation ID:
- 1175 to 1182
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Upon the secondary contact of populations, speciation with gene flow is greatly facilitated when the same pleiotropic loci are both subject to divergent ecological selection and induce non-random mating, leading to loci with this fortuitous combination of functions being referred to as ‘magic trait’ loci. We use a population genetics model to examine whether ‘pseudomagic trait’ complexes, composed of physically linked loci fulfilling these two functions, are as efficient in promoting premating isolation as magic traits. We specifically measure the evolution of choosiness, which controls the strength of assortative mating. We show that, surprisingly, pseudomagic trait complexes, and to a lesser extent also physically unlinked loci, can lead to the evolution of considerably stronger assortative mating preferences than do magic traits, provided polymorphism at the involved loci is maintained. This is because assortative mating preferences are generally favoured when there is a risk of producing maladapted recombinants, as occurs with non-magic trait complexes but not with magic traits (since pleiotropy precludes recombination). Contrary to current belief, magic traits may not be the most effective genetic architecture for promoting strong premating isolation. Therefore, distinguishing between magic traits and pseudomagic trait complexes is important when inferring their role in premating isolation. This calls for further fine-scale genomic research on speciation genes.more » « less
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Hybridization and subsequent genetic introgression are now known to be common features of the histories of many species, including our own. Following hybridization, selection often purges introgressed DNA genome-wide. While assortative mating can limit hybridization in the first place, it is also known to play an important role in postzygotic selection against hybrids and, thus, the purging of introgressed DNA. However, this role is usually thought of as a direct one: a tendency for mates to be conspecific reduces the sexual fitness of hybrids, reducing the transmission of introgressed ancestry. Here, we explore a second, indirect role of assortative mating as a postzygotic barrier to gene flow. Under assortative mating, parents covary in their ancestry, causing ancestry to be “bundled” in their offspring and later generations. This bundling effect increases ancestry variance in the population, enhancing the efficiency with which postzygotic selection purges introgressed DNA. Using whole-genome simulations, we show that the bundling effect can comprise a substantial portion of mate choice’s overall effect as a postzygotic barrier to gene flow. We then derive a simple method for estimating the impact of the bundling effect from standard metrics of assortative mating. Applying this method to data from a diverse set of hybrid zones, we find that the bundling effect increases the purging of introgressed DNA by between 1.2-fold (in a baboon system with weak assortative mating) and 14-fold (in a swordtail system with strong assortative mating). Thus, assortative mating’s bundling effect contributes substantially to the genetic isolation of species.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1111/jeb.14052
