As we uncover the ubiquity of hybridization in nature, determining how natural selection acts on hybrids has newfound importance for speciation. A study in PLOS Biology uses threespine stickleback to detect a genomic signature of ecological incompatibilities

Coughlan, Jenn

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PRIMEROne fish, two fish, red fish, dead fish:Detecting the genomic footprint of ecologicalincompatibilitiesJenn CoughlanID1,2*1 Biology Department, University of North Carolina, Chapel Hill, North Carolina, United States of America,2 Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, United Statesof America* jcoug@email.unc.eduAs we uncover the ubiquity of hybridization in nature, determininghow natural selection acts on hybrids has newfound importance forspeciation. A study in PLOS Biology uses threespine stickleback todetect a genomic signature of ecological incompatibilities.Selection against hybrids takes many formsA long-standing goal in evolutionary biology is to understand how natural selection acts onhybrids and assess how often selection against hybrids can contribute to reproductive isolationamong species. Selection against hybrids is often classified as intrinsic or extrinsic based onwhether hybrids exhibit low fitness across many environments or only in certain conditions,respectively [1]. These 2 mechanisms of selection against hybrids are also thought to have dif-ferent genetic architectures. Intrinsic incompatibilities largely arise through structural rear-rangements or multilocus incompatibilities, wherein novel allelic combinations in hybridshave an epistatic effect on fitness [1]. Extrinsic postzygotic isolation may stem from either anepistatic or additive genetic architecture. Most often, extrinsic barriers are discussed in termsof hybrid intermediacy, wherein hybrids exhibit intermediate phenotypes of locally importanttraits and are consequently maladapted to both parental environments (e.g., [2–4]). Yet,extrinsic barriers can also arise if multilocus genotypes give rise to transgressive traits or traitcombinations that are deleterious in certain environments.Although the idea that selection against hybrids may stem from these “ecological incompat-ibilities” is certainly not new [5], empirical examples are few and often involve F1 hybrids withmismatched traits. These mismatches may occur because which parent an F1 resembles candiffer between ecologically important traits (e.g., dominance mismatches [6]). Dominancemismatches are likely common between ecologically divergent species ([6]; examples include[7,8]). However, if the genetic architecture of ecological divergence is largely additive, traitmismatches may not manifest until recombination and independent assortment have reshuf-fled alleles to create individuals with alternate homozygous ancestry at 2 or more loci (akin toa fully recessive intrinsic incompatibility).While an intriguing possibility, the standard of evidence required to demonstrate suchcomplex extrinsic incompatibilities is substantial; researchers must generate hundreds of F2hybrids through manipulative crosses, rear replicate hybrid populations in multiplePLOS Biology | https://doi.org/10.1371/journal.pbio.3001504 January 11, 2022 1 / 4a1111111111a1111111111a1111111111a1111111111a1111111111OPEN ACCESSCitation: Coughlan J (2022) One fish, two fish, redfish, dead fish: Detecting the genomic footprint ofecological incompatibilities. PLoS Biol 20(1):e3001504. https://doi.org/10.1371/journal.pbio.3001504Published: January 11, 2022Copyright: © 2022 Jenn Coughlan. This is an openaccess article distributed under the terms of theCreative Commons Attribution License, whichpermits unrestricted use, distribution, andreproduction in any medium, provided the originalauthor and source are credited.Funding: JMC was supported by an NSF DEBDimensions of Biodiversity grant awarded to DanielMatute (DEB-DOB-1737752). The funders had norole in study design, data collection and analysis,decision to publish, or preparation of themanuscript.Competing interests: The authors have declaredthat no competing interests exist.environments, then track traits and fitness for each individual in each environment to generatefitness landscapes that are environment specific.Yet, selection against hybrids in an F2 generation is also predicted to leave distinct genomicsignatures. If particular combinations of homozygous genotypes lead to lowered fitness(whether intrinsically or through ecological selection; Fig 1; [9,10]), then when those individu-als are removed by natural selection, the surviving individuals will exhibit higher heterozygos-ity than expected at those particular loci. The more loci involved in the incompatibility, thestronger this genome-wide signature will be. This framework opens the door to a much sim-pler approach to detect ecological incompatibilities: Using ancestry-informative sites, compareheterozygosity of hybrids raised in the lab to those raised in natural conditions. If selection isecological, then only hybrids raised in natural conditions should exhibit excess ancestry het-erozygosity. The simplicity of this approach allows researchers to detect potential ecologicalincompatibilities in systems in which measuring multiple traits and tracking fitness per indi-vidual may be infeasible, or the specific traits involved are not obvious. Despite its promise,whether such signatures will be readily apparent at a coarse, genome-wide scale is largelyunknown (though see [10]).Identifying the genomic signatures of ecological incompatibilitiesIn this issue of PLOS Biology, Thompson and colleagues build on previous efforts in threespinestickleback (Gasterosteus aculeatus) by creatively leveraging previously published studies andunpublished data to look for genomic signatures of ecological incompatibilities [11]. Previouswork provided strong evidence that ecological selection against hybrids between limnetic andbenthic forms of threespine stickleback may be caused by trait mismatches [12]. In this system,the genetic architecture of divergence is complex, involving many small-effect and largelyadditive loci. Intriguingly, a subset of F2 hybrids exhibit unusual jaw morphologies that com-bine distinct traits from either parental species (rather than intermediate phenotypes, whichmost hybrids exhibit; [12]). These trait mismatches do not impede feeding in the lab, but whenraised in experimental ponds, these fish exhibit low feeding performance and consequentlysmall body size [12].To identify genome-wide signatures of ecological incompatibilities, Thompson and col-leagues calculated how much heterozygosity pond-raised and lab-raised hybrids exhibited, andhow much these levels of heterozygosity deviated from expected (i.e., excess ancestry heterozy-gosity [11]). Under a model of ecological incompatibilities, only the pond-raised hybridsshould exhibit excess ancestry heterozygosity ([10]; Fig 1). In line with this hypothesis, theauthors found that pond-raised hybrids were consistently more heterozygous at ancestry-informative sites, while lab-reared hybrids showed no deviations from expectation. Theirresults are robust; holding up across sequencing methods, studies, ponds, and even the paren-tal populations used to create the hybrids. Moreover, because field-specific heterozygosityexcess can be generated by several processes, the authors do a commendable job at ruling outalternative explanations, including field-specific heterosis and inbreeding depression. Thiswork represents a significant step forward for speciation genetics, presenting evidence for eco-logical incompatibilities in a model system and also providing a straightforward method fordetecting these types of incompatibilities in other systems.What, when, why, and how: Moving toward mechanism andassessing commonalityWith new tools in hand, what are the next steps for understanding ecological incompatibili-ties? While Thompson and colleagues present a straightforward method for detectingPLOS BIOLOGYPLOS Biology | https://doi.org/10.1371/journal.pbio.3001504 January 11, 2022 2 / 4ecological incompatibilities, amassing more examples will require substantial effort, and inmany systems will be unachievable. Nonetheless, as more examples of ecological incompatibil-ities accumulate, 2 key areas of research will emerge: What are the mechanisms underlyingecological incompatibilities and how important are they for speciation?Determining how selection acts on specific traits/trait combinations will be essential tounderstand how selection is acting against hybrids. This will require the nitty-gritty of buildingenvironment-specific fitness landscapes and tracking both the targets and agents of naturalselection in hybrid populations. Moreover, a comprehension of the genetic architecture of thetrait(s) involved in ecological incompatibilities will be a key step in elucidating the importanceof this reproductive barrier. UnderstandingAU : PleasecheckandconfirmthattheeditstothesentenceUnderstandingifthetraitsinvolvedinecologicalincompatibilitieshavelargely:::didnotaltertheintendedthoughtofthesentence:if the trait involved in ecological incompa ibilitieshave largely additive genetic architectures with epistatic effects on fitness, the number andFig 1. Ecological incompatibilities should leave a detectable genomic signature. F2 hybrids between 2 ecologically divergent species are raised in both benign lab andnatural or seminatural field environments. If the genetic architecture of divergence is largely additive, then most hybrids will exhibit an intermediate set of phenotypes.Yet, a subset of individuals with largely alternate homozygous ancestry at different loci may exhibit trait mismatches or transgressive traits (shown in purple). If theseindividuals are selected against, then heterozygosity of the surviving hybrids will be elevated relative to the expectation based on allele frequencies. Under a model ofecological incompatibility, this excess heterozygosity should be observed only in natural environments.https://doi.org/10.1371/journal.pbio.3001504.g001PLOS BIOLOGYPLOS Biology | https://doi.org/10.1371/journal.pbio.3001504 January 11, 2022 3 / 4effect size of the loci involved, and the strength of epistatic selection can give insight into howmuch of the genome is expected to be involved in reproductive isolation, as well as how manyhybrid individuals—and in what generation—low fitness is expected to manifest. The answersto these questions have crucial implications for the efficacy of ecological incompatibilities tolimiting gene flow in nature. LastlyAU : PleasecheckandconfirmthattheeditstothesentenceLastly; assessinghowcommonthesetypesofincompatibilitiesare and:::didnotaltertheintendedthoughtofthesentence:, assessing how ommon these types of incompatibilities areand when in the speciation process they tend to evolve are central for determining their impor-tance in speciation. The latter 2 goals will require amassing many examples of ecologicalincompatibilities, both across taxonomic groups as well as lineage pairs of differing divergencetimes within a group. While much work is needed, the creative reuse of previously publisheddatasets presented by Thompson and colleagues is a reminder that applying genomic technolo-gies to previous experiments may serve as a fruitful avenue forward.AcknowledgmentsThank you to Adam Stuckert and Andrius Dagilis for thoughtful comments.References1. Coughlan JM, Matute DR. The importance of intrinsic postzygotic barriers throughout the speciationprocess. Philos Trans R Soc Lond B Biol Sci. 2020; 375:20190533. https://doi.org/10.1098/rstb.2019.0533 PMID: 326546422. McBride CS, Singer MC. Field studies reveal strong postmating isolation between ecologically divergentbutterfly populations. PLoS Biol. 2010; 8:e1000529. https://doi.org/10.1371/journal.pbio.1000529PMID: 210489823. Delmore KE, Irwin DE. Hybrid songbirds employ intermediate routes in a migratory divide. Ecol Lett.2014; 17:1211–8. https://doi.org/10.1111/ele.12326 PMID: 250404564. DiVittorio CT, Singhal S, Roddy AB, Zapata F, Ackerly DD, Baldwin BG, et al. Natural selection main-tains species despite frequent hybridization in the desert shrub Encelia. Proc Natl Acad Sci U S A.2020; 117:33373–83. https://doi.org/10.1073/pnas.2001337117 PMID: 333181785. Dobzhansky T. Genetics and the Origin of Species. New York, NY: Columbia University Press; 1937.https://doi.org/10.1093/genetics/22.3.340 PMID: 172468456. Thompson KA, Urquhart-Cronish M, Whitney KD, Rieseberg LH, Schluter D. Patterns, Predictors, andConsequences of Dominance in Hybrids. Am Nat. 2021; 197:E72–88. https://doi.org/10.1086/712603PMID: 336259667. Coughlan JM, Brown MW, Willis JH. The genetic architecture and evolution of life-history divergenceamong perennials in the Mimulus guttatus species complex. Proc Biol Sci. 2021; 288:20210077. https://doi.org/10.1098/rspb.2021.0077 PMID: 338236718. Cooper BS, Sedghifar A, Nash WT, Comeault AA, Matute DR. A Maladaptive Combination of TraitsContributes to the Maintenance of a Drosophila Hybrid Zone. Curr Biol. 2018; 28:2940–2947.e6. https://doi.org/10.1016/j.cub.2018.07.005 PMID: 301741849. Barton NH, Gale KS. Genetic analysis of hybrid zones. Hybrid zones and the evolutionary process.1993;13–45.10. Simon A, Bierne N, Welch JJ. Coadapted genomes and selection on hybrids: Fisher’s geometric modelexplains a variety of empirical patterns. Evol Lett. 2018; 2:472–98. https://doi.org/10.1002/evl3.66PMID: 3028369611. Thompson KA, Peichel CL, Rennison DJ, Matthew D, McGee MD, Albert AYK, et al. Analysis of ances-try heterozygosity suggests that hybrid incompatibilities in threespine stickleback are environment-dependent. PLoS Biol. 2022; 20(1):e3001469.12. Arnegard ME, McGee MD, Metthews B, Marchinko KB, Conte GL, Kabir S, et al. Genetics of ecologicaldivergence during speciation. Nature. 2014; 511:307–11. https://doi.org/10.1038/nature13301 PMID:24909991PLOS BIOLOGYPLOS Biology | https://doi.org/10.1371/journal.pbio.3001504 January 11, 2022 4 / 4

One fish, two fish, red fish, dead fish: Detecting the genomic footprint of ecological incompatibilities

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One fish, two fish, red fish, dead fish: Detecting the genomic footprint of ecological incompatibilities

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