What is Speciation Genomics? The roles of ecology, gene flow, and genomic architecture in the formation of species

Campbell, C. Ryan; Poelstra, Jelmer W.; Yoder, Anne D.

doi:10.1093/biolinnean/bly063

Cited by 97 publications

(80 citation statements)

References 253 publications

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“…However, using genome 62 sequences from nine emerging species of monkeyflower coupled with simulations of 63 genomic divergence, we show that it is unlikely that background selection is the primary 64 architect of these landscapes. Rather, differentiation landscapes have probably been Introduction 71 The primary goal of speciation genomics is to interpret patterns of genome-wide 72 variation in light of the ecological and evolutionary processes that contribute to the origin 73 of new species (Ravinet et al 2017, Wolf and Ellegren 2017, Campbell et al 2018. 74 Advances in DNA sequencing now allow us to capture patterns of genome-wide variation 75 from organisms across the tree of life, but inferring the processes underlying these 76 patterns remains a formidable challenge (Ravinet et al 2017).…”

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confidence: 99%

Widespread selection and gene flow shape the genomic landscape during a radiation of monkeyflowers

Stankowski

Chase

Fuiten

et al. 2018

Preprint

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Speciation genomic studies aim to interpret patterns of genome-wide variation in light of the processes that give rise to new species. However, interpreting the genomic ‘landscape’ of speciation is difficult, because many evolutionary processes can impact levels of variation. Facilitated by the first chromosome-level assembly for the group, we use whole-genome sequencing and simulations to shed light on the processes that have shaped the genomic landscape during a recent radiation of monkeyflowers. After inferring the phylogenetic relationships among the nine taxa in this radiation, we show that highly similar diversity (π) and differentiation (FST) landscapes have emerged across the group. Variation in these landscapes was strongly predicted by the local density of functional elements and the recombination rate, suggesting that the landscapes have been shaped by widespread natural selection. Using the varying divergence times between pairs of taxa, we show that the correlations between FST and genome features arose almost immediately after a population split and have become stronger over time. Simulations of genomic landscape evolution suggest that background selection (i.e., selection against deleterious mutations) alone is too subtle to generate the observed patterns, but scenarios that involve positive selection and genetic incompatibilities are plausible alternative explanations. Finally, tests for introgression among these taxa reveal widespread evidence of heterogeneous selection against gene flow during this radiation. Thus, combined with existing evidence for adaptation in this system, we conclude that the correlation in FST among these taxa informs us about the genomic basis of adaptation and speciation in this system.Author summaryWhat can patterns of genome-wide variation tell us about the speciation process? The answer to this question depends upon our ability to infer the evolutionary processes underlying these patterns. This, however, is difficult, because many processes can leave similar footprints, but some have nothing to do with speciation per se. For example, many studies have found highly heterogeneous levels of genetic differentiation when comparing the genomes of emerging species. These patterns are often referred to as differentiation ‘landscapes’ because they appear as a rugged topography of ‘peaks’ and ‘valleys’ as one scans across the genome. It has often been argued that selection against deleterious mutations, a process referred to as background selection, is primarily responsible for shaping differentiation landscapes early in speciation. If this hypothesis is correct, then it is unlikely that patterns of differentiation will reveal much about the genomic basis of speciation. However, using genome sequences from nine emerging species of monkeyflower coupled with simulations of genomic divergence, we show that it is unlikely that background selection is the primary architect of these landscapes. Rather, differentiation landscapes have probably been shaped by adaptation and gene flow, which are processes that are central to our understanding of speciation. Therefore, our work has important implications for our understanding of what patterns of differentiation can tell us about the genetic basis of adaptation and speciation.

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Widespread selection and gene flow shape the genomic landscape during a radiation of monkeyflowers

Stankowski

Chase

Fuiten

et al. 2018

Preprint

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“…In this study, we found that for sympatric species with 583 high reproductive isolation, but low PPIL value, chromosomal rearrangement could be 584 implicated in the maintenance of species boundaries. Moreover, while chromosomal 585 rearrangements have long been associated with reproductive isolation and speciation (Rieseberg 586 2001;Campbell et al 2018), to our knowledge have not been formally investigated under a MSC 587 model. Supposing chromosomal inversions drive a rapid increase in reproductive isolation, the 588 effects of localized genomic islands of divergence may not extend throughout the genome or be 589 reflected in the few loci being used for delimitation.…”

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Model-based species delimitation: are coalescent species reproductively isolated?

Campillo

Barley

Thomson

2019

Preprint

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10A large and growing fraction of systematists define species as independently evolving lineages 11 that may be recognized by analyzing the population genetic history of alleles sampled from 12 individuals belonging to those species. This has motivated the development of increasingly 13 sophisticated statistical models rooted in the multispecies coalescent process. Specifically, these 14 models allow for simultaneous estimation of the number of species present in a sample of 15 individuals and the phylogenetic history of those species using only DNA sequence data from 16 independent loci. These methods hold extraordinary promise for increasing the efficiency of 17 species discovery, but require extensive validation to ensure that they are accurate and precise. 18Whether the species identified by these methods correspond to the species that would be 19 recognized by alternative species recognition criteria (such as measurements of reproductive 20 isolation) is currently an open question, and a subject of vigorous debate. Here we perform an 21 empirical test of these methods by making use of a classic model system in the history of 22 speciation research, flies of the genus Drosophila. Specifically, we use the uniquely 23 comprehensive data on reproductive isolation that is available for this system, along with DNA 24 sequence data, to ask whether Drosophila species inferred under the multispecies coalescent 25 model correspond to those recognized by many decades of speciation research. We found that 26 coalescent based and reproductive isolation based methods of inferring species boundaries are 27 concordant for 77% of the species pairs. We explore and discuss potential explanations for these 28 discrepancies. We also found that the amount of prezygotic isolation between two species is a 29 strong predictor of the posterior probability of species boundaries based on DNA sequence data, 30 regardless of whether the species pairs are sympatrically or allopatrically distributed. 31 or postzygotic isolation, and that value was greater than 0.95 or 1.0, respectively, we considered 126 T to equal the measure for which there was data (Coyne and Orr 1997). Conversely, if a species 127 pair only had data for prezygotic or postzygotic isolation, and that value was less than 0.95 or 128 1.0, respectively, those species pairs were excluded from downstream analysis. Data on allozyme 129 genetic distance (D) comes originally from Orr (1989, 1997), but more recently 130 updated by Yukilevich (2012). 131For the purpose of this study, we follow the species recognition thresholds proposed by 132Coyne and Orr (1997). Specifically, they proposed minimum values on total reproductive 133 isolation (T ³ 0.903) and genetic distance (sympatric pairs: D ³ 0.04; allopatric pairs: D ³ 0.54) 134 required for maintenance of species boundaries. While we recognize that the use of any 135 particular threshold may raise concerns, we opted to use these for two reasons. First, by using the 136

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“…The general role of natural selection per se is largely undisputed, but the population genetic details, especially the role of gene flow, continues to be hotly debated (Berlocher & Feder, 2002;Bird, Fernandez-Silva, Skillings, & Toonen, 2012;Bolnick & Fitzpatrick, 2007;Elmer, 2019;Mallet, Meyer, Nosil, & Feder, 2009). Indeed, theoretical studies of ecological speciation have recently focused on quantifying the combined effects of population genetic processes on genetic divergence, particularly the interplay of gene flow and divergent selection (Campbell, Poelstra, & Yoder, 2018;Nosil, 2012). Much of our knowledge of ecological speciation is based on a growing number of model and non-model organisms sampled sparsely across the tree of life including bacteria (Luo et al, 2011), fungi (Giraud, Refrégier, Le Gac, de Vienne, & Hood, 2008), plants (Macnair & Christie, 1983) and various insects (Egan et al, 2015;Nosil et al, 2018;Nouhaud et al, 2018).…”

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confidence: 99%

Host plant‐related genomic differentiation in the European cherry fruit fly, Rhagoletis cerasi

et al. 2019

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Elucidating the mechanisms and conditions facilitating the formation of biodiversity are central topics in evolutionary biology. A growing number of studies imply that divergent ecological selection may often play a critical role in speciation by counteracting the homogenising effects of gene flow. Several examples involve phytophagous insects, where divergent selection pressures associated with host plant shifts may generate reproductive isolation, promoting speciation. Here, we use ddRADseq to assess the population structure and to test for host‐related genomic differentiation in the European cherry fruit fly, Rhagoletis cerasi (L., 1758) (Diptera: Tephritidae). This tephritid is distributed throughout Europe and western Asia, and has adapted to two different genera of host plants, Prunus spp. (cherries) and Lonicera spp. (honeysuckle). Our data imply that geographic distance and geomorphic barriers serve as the primary factors shaping genetic population structure across the species range. Locally, however, flies genetically cluster according to host plant, with consistent allele frequency differences displayed by a subset of loci between Prunus and Lonicera flies across four sites surveyed in Germany and Norway. These 17 loci display significantly higher FST values between host plants than others. They also showed high levels of linkage disequilibrium within and between Prunus and Lonicera flies, supporting host‐related selection and reduced gene flow. Our findings support the existence of sympatric host races in R. cerasi embedded within broader patterns of geographic variation in the fly, similar to the related apple maggot, Rhagoletis pomonella, in North America.

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What is Speciation Genomics? The roles of ecology, gene flow, and genomic architecture in the formation of species

Cited by 97 publications

References 253 publications

Widespread selection and gene flow shape the genomic landscape during a radiation of monkeyflowers

Widespread selection and gene flow shape the genomic landscape during a radiation of monkeyflowers

Model-based species delimitation: are coalescent species reproductively isolated?

Host plant‐related genomic differentiation in the European cherry fruit fly, Rhagoletis cerasi

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