Behavioral Isolation due to Cascade Reinforcement in <i>Lucania</i> Killifish

Kozak, Genevieve M.; Roland, Genevieve; Rankhorn, Clare; Falater, Amy; Berdan, Emma L.; Fuller, Rebecca C.

doi:10.1086/680023

Cited by 46 publications

(71 citation statements)

References 63 publications

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“…Reinforcement in D. yakuba, therefore, adds to the growing number of examples demonstrating that locally adaptive phenotypes subject to reinforcing selection can have costs outside of regions of sympatry [18][19][20][21][22][23][24]. These examples provide evidence that the pattern of RCD frequently described in cases of reinforcement can be actively maintained by selection acting on 'reinforced' alleles between allopatric and sympatric conspecific populations.…”

Section: (B) Cascading Effects Of Reinforcementmentioning

confidence: 82%

“…the 'cascade reinforcement' hypothesis [14,15,17]). Recent work supports this hypothesis and suggests that phenotypes favoured by reinforcing selection in sympatry are often disadvantageous in allopatry [18][19][20][21][22][23]. The types of disadvantages can be diverse; however, because reinforcement frequently acts on traits involved in premating isolation, costs tend to manifest as a reduction in the ability to solicit potential mates when 'sympatric' phenotypes are found in allopatry [18][19][20][21][22]24].…”

Section: Introductionmentioning

confidence: 94%

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Correlated evolution of male and female reproductive traits drive a cascading effect of reinforcement inDrosophila yakuba

2016

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Selection against maladaptive hybridization can drive the evolution of reproductive isolation in a process called reinforcement. While the importance of reinforcement in evolution has been historically debated, many examples now exist. Despite these examples, we typically lack a detailed understanding of the mechanisms limiting the spread of reinforced phenotypes throughout a species' range. Here we address this issue in the fruit fly Drosophila yakuba, a species that hybridizes with its sister species D. santomea and is undergoing reinforcement in a well-defined hybrid zone on the island of São Tomé. Within this region, female D. yakuba show increased postmating-prezygotic (gametic) isolation towards D. santomea when compared with females from allopatric populations. We use a combination of natural collections, fertility assays, and experimental evolution to understand why reinforced gametic isolation in D. yakuba is confined to this hybrid zone. We show that, among other traits, D. yakuba males from sympatric populations sire fewer progeny than allopatric males when mated to allopatric D. yakuba females. Our results provide a novel example of reinforcement acting on a postmating-prezygotic trait in males, resulting in a cascade of reproductive isolation among conspecific populations.

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Section: (B) Cascading Effects Of Reinforcementmentioning

confidence: 82%

Section: Introductionmentioning

confidence: 94%

Correlated evolution of male and female reproductive traits drive a cascading effect of reinforcement inDrosophila yakuba

2016

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“…Evolution of reproductive barriers through reinforcement has been studied in a variety of organisms from killifish (Kozak et al. ), frogs (Lemmon ), and plants (Suni and Hopkins ) to several insect species (Noor ; Kronforst et al. ).…”

mentioning

confidence: 99%

“…Evolution of reproductive barriers through reinforcement has been studied in a variety of organisms from killifish (Kozak et al 2015), frogs (Lemmon 2009), and plants (Suni and Hopkins 2018) to several insect species (Noor 1999;Kronforst et al 2007). In Drosophila, sexual isolation has been shown to evolve faster than postzygotic isolation (Coyne and Orr 1997), and PMPZ isolation faster than hybrid inviability but more slowly than sexual isolation (Turissini et al 2018).…”

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confidence: 99%

Strength of sexual and postmating prezygotic barriers varies between sympatric populations with different histories and species abundances

et al. 2019

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The impact of different reproductive barriers on species or population isolation may vary in different stages of speciation depending on evolutionary forces acting within species and through species’ interactions. Genetic incompatibilities between interacting species are expected to reinforce prezygotic barriers in sympatric populations and lead to cascade reinforcement between conspecific populations living within and outside the areas of sympatry. We tested these predictions and studied whether and how the strength and target of reinforcement between Drosophila montana and Drosophila flavomontana vary between sympatric populations with different histories and species abundances. All barriers between D. montana females and D. flavomontana males were nearly complete, while in the reciprocal cross strong postzygotic isolation was accompanied by prezygotic barriers whose strength varied according to population composition. Sexual isolation between D. flavomontana females and D. montana males was increased in long‐established sympatric populations, where D. flavomontana is abundant, while postmating prezygotic (PMPZ) barriers were stronger in populations where this species is a new invader and still rare and where female discrimination against heterospecific males was lower. Strengthening of sexual and PMPZ barriers in this cross also induced cascade reinforcement of respective barriers between D. flavomontana populations, which is a classic signature of reinforcement process.

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“…While patterns of mate discrimination consistent with cascade reinforcement have been demonstrated in several empirical systems (Higgie & Blows, 2008;Hoskin, Higgie, McDonald, & Moritz, 2005;Jaenike, Dyer, Cornish, & Minhas, 2006;Kozak et al, 2015;Nosil, 2007;Saetre & Saether, 2010), much less is known about the conditions under which cascade reinforcement evolves (Fuller, 2016). Theoretical models by McPeek and Gavrilets (2006) and Pfennig and Ryan (2006) found that interactions with other species could alter female preferences to initiate isolation within species, but their models assumed speciation was nearly complete and no gene flow between sympatric and allopatric populations.…”

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confidence: 99%

Fine‐scale geographic patterns of gene flow and reproductive character displacement inDrosophila subquinariaandDrosophila recens

et al. 2018

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When two species are incompletely isolated, strengthening premating isolation barriers in response to the production of low fitness hybrids may complete the speciation process. Here, we use the sister species Drosophila subquinaria and Drosophila recens to study the conditions under which this reinforcement of species boundaries occurs in natural populations. We first extend the region of known sympatry between these species, and then we conduct a fine-scale geographic survey of mate discrimination coupled with estimates of gene flow within and admixture between species. Within D. subquinaria, reinforcement is extremely effective: we find variation in mate discrimination both against D. recens males and against conspecific allopatric males on the scale of a few kilometres and in the face of gene flow both from conspecific populations and introgression from D. recens. In D. recens, we do not find evidence for increased mate discrimination in sympatry, even where D. recens is rare, consistent with substantial gene flow throughout the species' range. Finally, we find that introgression between species is asymmetric, with more from D. recens into D. subquinaria than vice versa. Within each species, admixture is highest in the geographic region where it is rare relative to the other species, suggesting that when hybrids are produced they are of low fitness. In sum, reinforcement within D. subquinaria is effective at maintaining species boundaries, but even when reinforcing selection is strong it may not always result in a pattern of strong reproductive character displacement due to variation in the frequency of hybridization and gene flow from neighbouring populations.

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Behavioral Isolation due to Cascade Reinforcement in Lucania Killifish

Cited by 46 publications

References 63 publications

Correlated evolution of male and female reproductive traits drive a cascading effect of reinforcement inDrosophila yakuba

Correlated evolution of male and female reproductive traits drive a cascading effect of reinforcement inDrosophila yakuba

Strength of sexual and postmating prezygotic barriers varies between sympatric populations with different histories and species abundances

Fine‐scale geographic patterns of gene flow and reproductive character displacement inDrosophila subquinariaandDrosophila recens

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