In search of the Goldilocks zone for hybrid speciation

Abstract

Hybridization has recently gained considerable interest both as a unique opportunity for observing speciation mechanisms and as a potential engine for speciation. The latter remains a controversial topic. It was recently hypothesized that the reciprocal sorting of genetic incompatibilities from parental species could result in hybrid speciation, when the hybrid population maintains a mixed combination of the parental incompatibilities that prevents further gene exchange with both parental populations. However, the specifics of the purging/sorting process of multiple incompatibilities have not been examined theoretically. We here investigate the allele-frequency dynamics of an isolated hybrid population that results from a single hybridization event. Using models of two or four loci, we investigate the fate of one or two genetic incompatibilities of the Dobzhansky-Muller type (DMIs). We study how various parameters affect both the sorting/purging of the DMIs and the probability of observing hybrid speciation by reciprocal sorting. We find that the probability of hybrid speciation is strongly dependent on the linkage architecture (i.e. the order and recombination rate between loci along chromosomes), the population size of the hybrid population, and the initial relative contributions of the parental populations to the hybrid population. We identify a Goldilocks zone for specific linkage architectures and intermediate recombination rates, in which hybrid speciation becomes highly probable. Whereas an equal contribution of parental populations to the hybrid population maximizes the hybrid speciation probability in the Goldilocks zone, other linkage architectures yield unintuitive asymmetric maxima. We provide an explanation for this pattern, and discuss our results both with respect to the best conditions for observing hybrid speciation in nature and their implications regarding patterns of introgression in hybrid zones.

The contribution of ancient admixture to reproductive isolation between European sea bass lineages

“…The resulting genomic architecture of RI between contemporary D. labrax lineages is thus constituted by a mosaic of fixed blocks of different ancestries, that is, a mixture of genetic barriers inherited from the divergence history particular to D. labrax and the contribution of ancient admixture. Although additional analyses will be needed to fully understand which process has driven the fixation of D. punctatus alleles within Atlantic genomes, the resolution of genetic conflicts between D. punctatus and D. labrax seems the most parsimonious hypothesis (Schumer et al 2015; Blanckaert and Bank 2018). This speciation mechanism can be thought of as a transfer of incompatibilities between two species boundaries, from the strongest to the weakest barrier, which is eventually strengthened by the displacement of genetic conflicts inherited from an ancient episode of admixture.…”

“…Reproductive isolation may also have evolved through the resolution of genetic conflicts resulting from the contact between two diverged populations (Schumer et al 2015; Blanckaert and Bank 2018). Because each population has almost inevitably fixed new adaptive or nearly neutral variants that form incompatibilities when combined in hybrid genomes (Dobzhansky 1937), Bateson‐Dobzhansky‐Muller incompatibilities (BDMIs) are recognized as a common substrate for speciation (Presgraves 2010).…”

TallPinus luzmariaetrees with genes fromP. herrerae

“…It can also act as an additional, perhaps more abundant, source of adaptive genetic variation than mutation (Grant & Grant, 1994), by allowing gene flow and recombination (Abbott et al, 2013;Hipp, 2018). Furthermore, hybridization is one of the key sources of species formation and diversity, and many species may have originated by this route (Linder & Risenberg, 2004;Blanckaert & Bank, 2018), perhaps even as much as between 30% and 80% of all species (Wendel, McD & Rettig, 1991). On the other hand, increasing rates of hybridization may also lead to the extinction of unique populations or species because of unsuccessful reproductive efforts or introgression with a more common species (Rhymer & Simberloff, 1996;Blanckaert & Bank, 2018).…”

Peer Review #1 of "Tall Pinus luzmariae trees with genes from P. herrerae (v0.2)"

“…It can also act as an additional, perhaps more abundant, source of adaptive genetic variation than mutation (Grant & Grant 1994), by allowing gene flow and recombination (Abbott et al, 2013;Hipp, 2018). Furthermore, hybridization is one of the key sources of species formation and diversity, and many species may have originated by this route (Linder & Risenberg, 2004;Blanckaert & Bank, 2018), perhaps even as much as between 30% and 80% of all species (Wendel et al, 1991). On the other hand, increasing rates of hybridization may also lead to the extinction of unique populations or species because of unsuccessful reproductive efforts or introgression with a more common species (Rhymer & Simberloff, 1996;Blanckaert & Bank, 2018).…”

“…Furthermore, hybridization is one of the key sources of species formation and diversity, and many species may have originated by this route (Linder & Risenberg, 2004;Blanckaert & Bank, 2018), perhaps even as much as between 30% and 80% of all species (Wendel et al, 1991). On the other hand, increasing rates of hybridization may also lead to the extinction of unique populations or species because of unsuccessful reproductive efforts or introgression with a more common species (Rhymer & Simberloff, 1996;Blanckaert & Bank, 2018). In times of rapid ongoing climate change, hybridization may thus contribute to further extinctions, sometimes weakening reproductive isolation among species (Owens & Samuk, 2019) as well as supporting the development of novel segregating genotypes that will speed up adaptation to changes in climate (Chunco, 2014;Menon et al, 2019).…”