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1. The roles of recombination and selection in shaping genomic divergence in an incipient ecological species complex

   https://doi.org/10.1111/mec.16383  

   Wersebe, Matthew J. ; Sherman, Ryan E. ; Jeyasingh, Punidan D. ; Weider, Lawrence J. ( February 2022 , Molecular Ecology)

   Speciation genomic studies have revealed that genomes of diverging lineages are shaped jointly by the actions of gene flow and selection. These evolutionary forces acting in concert with processes such as recombination and genome features such as gene density shape a mosaic landscape of divergence. We investigated the roles of recombination and gene density in shaping the patterns of differentiation and divergence between the cyclically parthenogenetic ecological sister‐taxa,Daphnia pulicariaandDaphnia pulex. First, we assembled a phased chromosome‐scale genome assembly using trio‐binning forD.pulicariaand constructed a genetic map using an F2‐intercross panel to understand sex‐specific recombination rate heterogeneity. Finally, we used a ddRADseq data set with broad geographic sampling ofD.pulicaria,D.pulex, and their hybrids to understand the patterns of genome‐scale divergence and demographic parameters. Our study provides the first sex‐specific estimates of recombination rates for a cyclical parthenogen, and unlike other eukaryotic species, we observed male‐biased heterochiasmy inD.pulicaria, which may be related to this somewhat unique breeding mode. Additionally, regions of high gene density and recombination are generally more divergent than regions of suppressed recombination. Outlier analysis indicated that divergent genomic regions are probably driven by selection onD.pulicaria, the derived lineage colonizing a novel lake habitat. Together, our study supports a scenario of selection acting on genes related to local adaptation shaping genome‐wide patterns of differentiation despite high local recombination rates in this species complex. Finally, we discuss the limitations of our data in light of demographic uncertainty.

    

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2. Reproductive isolation and introgression between sympatric Mimulus species

   https://doi.org/10.1111/mec.13630  

   Kenney, Amanda M. ; Sweigart, Andrea L. ( May 2016 , Molecular Ecology)

   Incompletely isolated species provide an opportunity to investigate the genetic mechanisms and evolutionary forces that maintain distinct species in the face of ongoing gene flow. Here, we use field surveys and reduced representation sequencing to characterize the patterns of reproductive isolation, admixture and genomic divergence between populations of the outcrossing wildflowerMimulus guttatusand selfingM. nasutus. Focusing on a single site where these two species have come into secondary contact, we find that phenological isolation is strong, although incomplete, and is likely driven by divergence in response to photoperiod. In contrast to previous field studies, which have suggested that F₁‐hybrid formation might be rare, we discover patterns of genomic variation consistent with ongoing introgression. Strikingly, admixed individuals vary continuously from highly admixed to nearly pureM. guttatus, demonstrating ongoing hybridization and asymmetric introgression fromM. nasutusintoM. guttatus. Patterns of admixture and divergence across the genome show that levels of introgression are more variable than expected by chance. Some genomic regions show a reduced introgression, including one region that overlaps a critical photoperiodQTL, whereas other regions show elevated levels of interspecific gene flow. In addition, we observe a genome‐wide negative relationship between absolute divergence and the local recombination rate, potentially indicating natural selection againstM. nasutusancestry inM. guttatusgenetic backgrounds. Together, our results suggest thatMimulusspeciation is both ongoing and dynamic and that a combination of divergence in phenology and mating system, as well as selection against interspecific alleles, likely maintains these sympatric species.

    

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3. Genomic islands of differentiation in a rapid avian radiation have been driven by recent selective sweeps

   https://doi.org/10.1073/pnas.2015987117  

   Hejase, Hussein A. ; Salman-Minkov, Ayelet ; Campagna, Leonardo ; Hubisz, Melissa J. ; Lovette, Irby J. ; Gronau, Ilan ; Siepel, Adam ( November 2020 , Proceedings of the National Academy of Sciences)

   Numerous studies of emerging species have identified genomic “islands” of elevated differentiation against a background of relative homogeneity. The causes of these islands remain unclear, however, with some signs pointing toward “speciation genes” that locally restrict gene flow and others suggesting selective sweeps that have occurred within nascent species after speciation. Here, we examine this question through the lens of genome sequence data for five species of southern capuchino seedeaters, finch-like birds from South America that have undergone a species radiation during the last ∼50,000 generations. By applying newly developed statistical methods for ancestral recombination graph inference and machine-learning methods for the prediction of selective sweeps, we show that previously identified islands of differentiation in these birds appear to be generally associated with relatively recent, species-specific selective sweeps, most of which are predicted to be soft sweeps acting on standing genetic variation. Many of these sweeps coincide with genes associated with melanin-based variation in plumage, suggesting a prominent role for sexual selection. At the same time, a few loci also exhibit indications of possible selection against gene flow. These observations shed light on the complex manner in which natural selection shapes genome sequences during speciation.

    

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4. Incomplete reproductive isolation and low genetic differentiation despite floral divergence across varying geographic scales in Castilleja

   https://doi.org/10.1002/ajb2.1700  

   Wenzell, Katherine E. ; McDonnell, Angela J. ; Wickett, Norman J. ; Fant, Jeremie B. ; Skogen, Krissa A. ( July 2021 , American Journal of Botany)

   Divergence depends on the strength of selection and frequency of gene flow between taxa, while reproductive isolation relies on mating barriers and geographic distance. Less is known about how these processes interact at early stages of speciation. Here, we compared population‐level differentiation in floral phenotype and genetic sequence variation among recently divergedCastillejato explore patterns of diversification under different scenarios of reproductive isolation.

   Using target enrichment enabled by the Angiosperms353 probe set, we assessed genetic distance among 50 populations of fourCastillejaspecies. We investigated whether patterns of genetic divergence are explained by floral trait variation or geographic distance in two focal groups: the widespreadC. sessilifloraand the more restrictedC. purpureaspecies complex.

   We document thatC. sessilifloraand theC. purpureacomplex are characterized by high diversity in floral color across varying geographic scales. Despite phenotypic divergence, groups were not well supported in phylogenetic analyses, and little genetic differentiation was found across targeted Angiosperms353 loci. Nonetheless, a principal coordinate analysis of single nucleotide polymorphisms revealed differentiation withinC. sessilifloraacross floral morphs and geography and less differentiation among species of theC. purpureacomplex.

   Patterns of genetic distance inC. sessiliflorasuggest species cohesion maintained over long distances despite variation in floral traits. In theC. purpureacomplex, divergence in floral color across narrow geographic clines may be driven by recent selection on floral color. These contrasting patterns of floral and genetic differentiation reveal that divergence can arise via multiple eco‐evolutionary paths.

    

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5. A genomic timescale for placental mammal evolution

   https://doi.org/10.1126/science.abl8189  

   Foley, Nicole M. ; Mason, Victor C. ; Harris, Andrew J. ; Bredemeyer, Kevin R. ; Damas, Joana ; Lewin, Harris A. ; Eizirik, Eduardo ; Gatesy, John ; Karlsson, Elinor K. ; Lindblad-Toh, Kerstin ; et al ( April 2023 , Science)

   INTRODUCTION Resolving the role that different environmental forces may have played in the apparent explosive diversification of modern placental mammals is crucial to understanding the evolutionary context of their living and extinct morphological and genomic diversity. RATIONALE Limited access to whole-genome sequence alignments that sample living mammalian biodiversity has hampered phylogenomic inference, which until now has been limited to relatively small, highly constrained sequence matrices often representing <2% of a typical mammalian genome. To eliminate this sampling bias, we used an alignment of 241 whole genomes to comprehensively identify and rigorously analyze noncoding, neutrally evolving sequence variation in coalescent and concatenation-based phylogenetic frameworks. These analyses were followed by validation with multiple classes of phylogenetically informative structural variation. This approach enabled the generation of a robust time tree for placental mammals that evaluated age variation across hundreds of genomic loci that are not restricted by protein coding annotations. RESULTS Coalescent and concatenation phylogenies inferred from multiple treatments of the data were highly congruent, including support for higher-level taxonomic groupings that unite primates+colugos with treeshrews (Euarchonta), bats+cetartiodactyls+perissodactyls+carnivorans+pangolins (Scrotifera), all scrotiferans excluding bats (Fereuungulata), and carnivorans+pangolins with perissodactyls (Zooamata). However, because these approaches infer a single best tree, they mask signatures of phylogenetic conflict that result from incomplete lineage sorting and historical hybridization. Accordingly, we also inferred phylogenies from thousands of noncoding loci distributed across chromosomes with historically contrasting recombination rates. Throughout the radiation of modern orders (such as rodents, primates, bats, and carnivores), we observed notable differences between locus trees inferred from the autosomes and the X chromosome, a pattern typical of speciation with gene flow. We show that in many cases, previously controversial phylogenetic relationships can be reconciled by examining the distribution of conflicting phylogenetic signals along chromosomes with variable historical recombination rates. Lineage divergence time estimates were notably uniform across genomic loci and robust to extensive sensitivity analyses in which the underlying data, fossil constraints, and clock models were varied. The earliest branching events in the placental phylogeny coincide with the breakup of continental landmasses and rising sea levels in the Late Cretaceous. This signature of allopatric speciation is congruent with the low genomic conflict inferred for most superordinal relationships. By contrast, we observed a second pulse of diversification immediately after the Cretaceous-Paleogene (K-Pg) extinction event superimposed on an episode of rapid land emergence. Greater geographic continuity coupled with tumultuous climatic changes and increased ecological landscape at this time provided enhanced opportunities for mammalian diversification, as depicted in the fossil record. These observations dovetail with increased phylogenetic conflict observed within clades that diversified in the Cenozoic. CONCLUSION Our genome-wide analysis of multiple classes of sequence variation provides the most comprehensive assessment of placental mammal phylogeny, resolves controversial relationships, and clarifies the timing of mammalian diversification. We propose that the combination of Cretaceous continental fragmentation and lineage isolation, followed by the direct and indirect effects of the K-Pg extinction at a time of rapid land emergence, synergistically contributed to the accelerated diversification rate of placental mammals during the early Cenozoic. The timing of placental mammal evolution. Superordinal mammalian diversification took place in the Cretaceous during periods of continental fragmentation and sea level rise with little phylogenomic discordance (pie charts: left, autosomes; right, X chromosome), which is consistent with allopatric speciation. By contrast, the Paleogene hosted intraordinal diversification in the aftermath of the K-Pg mass extinction event, when clades exhibited higher phylogenomic discordance consistent with speciation with gene flow and incomplete lineage sorting. 

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