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1. Ancient hybridization leads to the repeated evolution of red flowers across a monkeyflower radiation

   https://doi.org/10.1093/evlett/qrad024  

   Short, Aidan W.; Streisfeld, Matthew A. (June 2023, Evolution Letters)

   Abstract The reuse of old genetic variation can promote rapid diversification in evolutionary radiations, but in most cases, the historical events underlying this divergence are not known. For example, ancient hybridization can generate new combinations of alleles that sort into descendant lineages, potentially providing the raw material to initiate divergence. In the Mimulus aurantiacus species complex, there is evidence for widespread gene flow among members of this radiation. In addition, allelic variation in the MaMyb2 gene is responsible for differences in flower color between the closely related ecotypes of subspecies puniceus, contributing to reproductive isolation by pollinators. Previous work suggested that MaMyb2 was introgressed into the red-flowered ecotype of puniceus. However, additional taxa within the radiation have independently evolved red flowers from their yellow-flowered ancestors, raising the possibility that this introgression had a more ancient origin. In this study, we used repeated tests of admixture from whole-genome sequence data across this diverse radiation to demonstrate that there has been both ancient and recurrent hybridization in this group. However, most of the signal of this ancient introgression has been removed due to selection, suggesting that widespread barriers to gene flow are in place between taxa. Yet, a roughly 30 kb region that contains the MaMyb2 gene is currently shared only among the red-flowered taxa. Patterns of admixture, sequence divergence, and extended haplotype homozygosity across this region confirm a history of ancient hybridization, where functional variants have been preserved due to positive selection in red-flowered taxa but lost in their yellow-flowered counterparts. The results of this study reveal that selection against gene flow can reduce genomic signatures of ancient hybridization, but that historical introgression can provide essential genetic variation that facilitates the repeated evolution of phenotypic traits between lineages. 

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2. Divergent diapause life history timing drives both allochronic speciation and reticulate hybridization in an adaptive radiation of Rhagoletis flies

   https://doi.org/10.1111/mec.15908  

   Inskeep, Katherine_A; Doellman, Meredith_M; Powell, Thomas_H_Q; Berlocher, Stewart_H; Seifert, Nicholas_R; Hood, Glen_R; Ragland, Gregory_J; Meyers, Peter_J; Feder, Jeffrey_L (April 2021, Molecular Ecology)

   Abstract Divergent adaptation to new ecological opportunities can be an important factor initiating speciation. However, as niches are filled during adaptive radiations, trait divergence driving reproductive isolation between sister taxa may also result in trait convergence with more distantly related taxa, increasing the potential for reticulated gene flow across the radiation. Here, we demonstrate such a scenario in a recent adaptive radiation ofRhagoletisfruit flies, specialized on different host plants. Throughout this radiation, shifts to novel hosts are associated with changes in diapause life history timing, which act as “magic traits” generating allochronic reproductive isolation and facilitating speciation‐with‐gene‐flow. Evidence from laboratory rearing experiments measuring adult emergence timing and genome‐wide DNA‐sequencing surveys supported allochronic speciation between summer‐fruitingVacciniumspp.‐infestingRhagoletis mendaxand its hypothesized and undescribed sister taxon infesting autumn‐fruiting sparkleberries. The sparkleberry fly andR. mendaxwere shown to be genetically discrete sister taxa, exhibiting no detectable gene flow and allochronically isolated by a 2‐month average difference in emergence time corresponding to host availability. At sympatric sites across the southern USA, the later fruiting phenology of sparkleberries overlaps with that of flowering dogwood, the host of another more distantly related and undescribedRhagoletistaxon. Laboratory emergence data confirmed broadly overlapping life history timing and genomic evidence supported on‐going gene flow between sparkleberry and flowering dogwood flies. Thus, divergent phenological adaptation can drive the initiation of reproductive isolation, while also enhancing genetic exchange across broader adaptive radiations, potentially serving as a source of novel genotypic variation and accentuating further diversification. 

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3. Geogenomic Predictors of Genetree Heterogeneity Explain Phylogeographic and Introgression History: A Case Study in an Amazonian Bird ( Thamnophilus aethiops )

   https://doi.org/10.1093/sysbio/syad061  

   Musher, Lukas_J; Del-Rio, Glaucia; Marcondes, Rafael_S; Brumfield, Robb_T; Bravo, Gustavo_A; Thom, Gregory; Burbrink, ed., Frank (October 2023, Systematic Biology)

   Abstract Can knowledge about genome architecture inform biogeographic and phylogenetic inference? Selection, drift, recombination, and gene flow interact to produce a genomic landscape of divergence wherein patterns of differentiation and genealogy vary nonrandomly across the genomes of diverging populations. For instance, genealogical patterns that arise due to gene flow should be more likely to occur on smaller chromosomes, which experience high recombination, whereas those tracking histories of geographic isolation (reduced gene flow caused by a barrier) and divergence should be more likely to occur on larger and sex chromosomes. In Amazonia, populations of many bird species diverge and introgress across rivers, resulting in reticulated genomic signals. Herein, we used reduced representation genomic data to disentangle the evolutionary history of 4 populations of an Amazonian antbird, Thamnophilus aethiops, whose biogeographic history was associated with the dynamic evolution of the Madeira River Basin. Specifically, we evaluate whether a large river capture event ca. 200 Ka, gave rise to reticulated genealogies in the genome by making spatially explicit predictions about isolation and gene flow based on knowledge about genomic processes. We first estimated chromosome-level phylogenies and recovered 2 primary topologies across the genome. The first topology (T1) was most consistent with predictions about population divergence and was recovered for the Z-chromosome. The second (T2), was consistent with predictions about gene flow upon secondary contact. To evaluate support for these topologies, we trained a convolutional neural network to classify our data into alternative diversification models and estimate demographic parameters. The best-fit model was concordant with T1 and included gene flow between non-sister taxa. Finally, we modeled levels of divergence and introgression as functions of chromosome length and found that smaller chromosomes experienced higher gene flow. Given that (1) genetrees supporting T2 were more likely to occur on smaller chromosomes and (2) we found lower levels of introgression on larger chromosomes (and especially the Z-chromosome), we argue that T1 represents the history of population divergence across rivers and T2 the history of secondary contact due to barrier loss. Our results suggest that a significant portion of genomic heterogeneity arises due to extrinsic biogeographic processes such as river capture interacting with intrinsic processes associated with genome architecture. Future phylogeographic studies would benefit from accounting for genomic processes, as different parts of the genome reveal contrasting, albeit complementary histories, all of which are relevant for disentangling the intricate geogenomic mechanisms of biotic diversification. [Amazonia; biogeography; demographic modeling; gene flow; gene tree; genome architecture; geogenomics; introgression; linked selection; neural network; phylogenomic; phylogeography; reproductive isolation; speciation; species tree.] 

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4. Strong postmating reproductive isolation in Mimulus section Eunanus

   https://doi.org/10.1111/jeb.14219  

   Farnitano, Matthew C.; Sweigart, Andrea L. (October 2023, Journal of Evolutionary Biology)

   Abstract Postmating reproductive isolation can help maintain species boundaries when premating barriers to reproduction are incomplete. The strength and identity of postmating reproductive barriers are highly variable among diverging species, leading to questions about their genetic basis and evolutionary drivers. These questions have been tackled in model systems but are less often addressed with broader phylogenetic resolution. In this study we analyse patterns of genetic divergence alongside direct measures of postmating reproductive barriers in an overlooked group of sympatric species within the model monkeyflower genus, Mimulus. Within this Mimulus brevipes species group, we find substantial divergence among species, including a cryptic genetic lineage. However, rampant gene discordance and ancient signals of introgression suggest a complex history of divergence. In addition, we find multiple strong postmating barriers, including postmating prezygotic isolation, hybrid seed inviability and hybrid male sterility. M. brevipes and M. fremontii have substantial but incomplete postmating isolation. For all other tested species pairs, we find essentially complete postmating isolation. Hybrid seed inviability appears linked to differences in seed size, providing a window into possible developmental mechanisms underlying this reproductive barrier. While geographic proximity and incomplete mating isolation may have allowed gene flow within this group in the distant past, strong postmating reproductive barriers today have likely played a key role in preventing ongoing introgression. By producing foundational information about reproductive isolation and genomic divergence in this understudied group, we add new diversity and phylogenetic resolution to our understanding of the mechanisms of plant speciation. Abstract Hybrid seed inviability and other postmating reproductive barriers isolate species in Mimulus section Eunanus. Variation in seed size may help explain hybrid seed failure. Whole-genome sequencing indicates a complex history of divergence, including signals of ancient introgression and cryptic diversity. 

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5. Genomic architecture and introgression shape a butterfly radiation

   https://doi.org/10.1126/science.aaw2090  

   Edelman, Nathaniel B.; Frandsen, Paul B.; Miyagi, Michael; Clavijo, Bernardo; Davey, John; Dikow, Rebecca B.; García-Accinelli, Gonzalo; Van Belleghem, Steven M.; Patterson, Nick; Neafsey, Daniel E.; et al (October 2019, Science)

   We used 20 de novo genome assemblies to probe the speciation history and architecture of gene flow in rapidly radiatingHeliconiusbutterflies. Our tests to distinguish incomplete lineage sorting from introgression indicate that gene flow has obscured several ancient phylogenetic relationships in this group over large swathes of the genome. Introgressed loci are underrepresented in low-recombination and gene-rich regions, consistent with the purging of foreign alleles more tightly linked to incompatibility loci. Here, we identify a hitherto unknown inversion that traps a color pattern switch locus. We infer that this inversion was transferred between lineages by introgression and is convergent with a similar rearrangement in another part of the genus. These multiple de novo genome sequences enable improved understanding of the importance of introgression and selective processes in adaptive radiation. 

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