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1. Ancient and recent introgression shape the evolutionary history of pollinator adaptation and speciation in a model monkeyflower radiation (Mimulus section Erythranthe)

   https://doi.org/10.1371/journal.pgen.1009095  

   Nelson, Thomas C. ; Stathos, Angela M. ; Vanderpool, Daniel D. ; Finseth, Findley R. ; Yuan, Yao-wu ; Fishman, Lila ( February 2021 , PLOS Genetics)

   Buerkle, Alex (Ed.)

   Inferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species ) . Taxa within Erythranthe , particularly the parapatric and putatively sister species M . lewisii (bee-pollinated) and M . cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M . cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M . lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele sharing (Patterson’s D-statistic and related tests) indicate that gene tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination andmore »adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M . lewisii and M . cardinalis . Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M . lewisii and Southern Californian M . parishii each carrying organelle genomes nested within respective sympatric M . cardinalis clades. A recent organellar transfer from M . cardinalis , an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M . parishii organelles in hybrids with M . lewisii . Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation.« less
2. The roles of hybridization and habitat fragmentation in the evolution of Brazil’s enigmatic longwing butterflies, Heliconius nattereri and H. hermathena

   https://doi.org/10.1186/s12915-020-00797-1  

   Massardo, Darli ; VanKuren, Nicholas W. ; Nallu, Sumitha ; Ramos, Renato R. ; Ribeiro, Pedro G. ; Silva-Brandão, Karina L. ; Brandão, Marcelo M. ; Lion, Marília B. ; Freitas, André V. ; Cardoso, Márcio Z. ; et al ( December 2020 , BMC Biology)

   Abstract Background Heliconius butterflies are widely distributed across the Neotropics and have evolved a stunning array of wing color patterns that mediate Müllerian mimicry and mating behavior. Their rapid radiation has been strongly influenced by hybridization, which has created new species and allowed sharing of color patterning alleles between mimetic species pairs. While these processes have frequently been observed in widespread species with contiguous distributions, many Heliconius species inhabit patchy or rare habitats that may strongly influence the origin and spread of species and color patterns. Here, we assess the effects of historical population fragmentation and unique biology on the origins, genetic health, and color pattern evolution of two rare and sparsely distributed Brazilian butterflies, Heliconius hermathena and Heliconius nattereri . Results We assembled genomes and re-sequenced whole genomes of eight H. nattereri and 71 H. hermathena individuals. These species harbor little genetic diversity, skewed site frequency spectra, and high deleterious mutation loads consistent with recent population bottlenecks. Heliconius hermathena consists of discrete, strongly isolated populations that likely arose from a single population that dispersed after the last glacial maximum. Despite having a unique color pattern combination that suggested a hybrid origin, we found no genome-wide evidence that H. hermathenamore »is a hybrid species. However, H. hermathena mimicry evolved via introgression, from co-mimetic Heliconius erato , of a small genomic region upstream of the color patterning gene cortex . Conclusions Heliconius hermathena and H. nattereri population fragmentation, potentially driven by historical climate change and recent deforestation, has significantly reduced the genetic health of these rare species. Our results contribute to a growing body of evidence that introgression of color patterning alleles between co-mimetic species appears to be a general feature of Heliconius evolution.« less
3. Mitochondrial Ecophysiology: Assessing the Evolutionary Forces That Shape Mitochondrial Variation

   https://doi.org/10.1093/icb/icz124  

   McKenzie, Jessica L. ; Chung, Dillon J. ; Healy, Timothy M. ; Brennan, Reid S. ; Bryant, Heather J. ; Whitehead, Andrew ; Schulte, Patricia M. ( July 2019 , Integrative and Comparative Biology)

   The mitonuclear species concept hypothesizes that incompatibilities between interacting gene products of the nuclear and mitochondrial genomes are a major factor establishing and maintaining species boundaries. However, most of the data available to test this concept come from studies of genetic variation in mitochondrial DNA, and clines in the mitochondrial genome across contact zones can be produced by a variety of forces. Here, we show that using a combination of population genomic analyses of the nuclear and mitochondrial genomes and studies of mitochondrial function can provide insight into the relative roles of neutral processes, adaptive evolution, and mitonuclear incompatibility in establishing and maintaining mitochondrial clines, using Atlantic killifish (Fundulus heteroclitus) as a case study. There is strong evidence for a role of secondary contact following the last glaciation in shaping a steep mitochondrial cline across a contact zone between northern and southern subspecies of killifish, but there is also evidence for a role of adaptive evolution in driving differentiation between the subspecies in a variety of traits from the level of the whole organism to the level of mitochondrial function. In addition, studies are beginning to address the potential for mitonuclear incompatibilities in admixed populations. However, population genomic studiesmore »have failed to detect evidence for a strong and pervasive influence of mitonuclear incompatibilities, and we suggest that polygenic selection may be responsible for the complex patterns observed. This case study demonstrates that multiple forces can act together in shaping mitochondrial clines, and illustrates the challenge of disentangling their relative roles.

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4. Novel trends of genome evolution in highly complex tropical sponge microbiomes

   https://doi.org/10.1186/s40168-022-01359-z  

   Kelly, Joseph B. ; Carlson, David E. ; Low, Jun Siong ; Thacker, Robert W. ( December 2022 , Microbiome)

   Abstract Background Tropical members of the sponge genus Ircinia possess highly complex microbiomes that perform a broad spectrum of chemical processes that influence host fitness. Despite the pervasive role of microbiomes in Ircinia biology, it is still unknown how they remain in stable association across tropical species. To address this question, we performed a comparative analysis of the microbiomes of 11 Ircinia species using whole-metagenomic shotgun sequencing data to investigate three aspects of bacterial symbiont genomes—the redundancy in metabolic pathways across taxa, the evolution of genes involved in pathogenesis, and the nature of selection acting on genes relevant to secondary metabolism. Results A total of 424 new, high-quality bacterial metagenome-assembled genomes (MAGs) were produced for 10 Caribbean Ircinia species, which were evaluated alongside 113 publicly available MAGs sourced from the Pacific species Ircinia ramosa . Evidence of redundancy was discovered in that the core genes of several primary metabolic pathways could be found in the genomes of multiple bacterial taxa. Across hosts, the metagenomes were depleted in genes relevant to pathogenicity and enriched in eukaryotic-like proteins (ELPs) that likely mimic the hosts’ molecular patterning. Finally, clusters of steroid biosynthesis genes (CSGs), which appear to be under purifying selection and undergomore »horizontal gene transfer, were found to be a defining feature of Ircinia metagenomes. Conclusions These results illustrate patterns of genome evolution within highly complex microbiomes that illuminate how associations with hosts are maintained. The metabolic redundancy within the microbiomes could help buffer the hosts from changes in the ambient chemical and physical regimes and from fluctuations in the population sizes of the individual microbial strains that make up the microbiome. Additionally, the enrichment of ELPs and depletion of LPS and cellular motility genes provide a model for how alternative strategies to virulence can evolve in microbiomes undergoing mixed-mode transmission that do not ultimately result in higher levels of damage (i.e., pathogenicity) to the host. Our last set of results provides evidence that sterol biosynthesis in Ircinia -associated bacteria is widespread and that these molecules are important for the survival of bacteria in highly complex Ircinia microbiomes.« less
5. The Genomic Landscapes of Desert Birds Form over Multiple Time Scales

   https://doi.org/10.1093/molbev/msac200  

   Provost, Kaiya ; Shue, Stephanie Yun ; Forcellati, Meghan ; Smith, Brian Tilston ; Yoder, ed., Anne ( September 2022 , Molecular Biology and Evolution)

   Spatial models show that genetic differentiation between populations can be explained by factors ranging from geographic distance to environmental resistance across the landscape. However, genomes exhibit a landscape of differentiation, indicating that multiple processes may mediate divergence in different portions of the genome. We tested this idea by comparing alternative geographic predctors of differentiation in ten bird species that co-occur in Sonoran and Chihuahuan Deserts of North America. Using population-level genomic data, we described the genomic landscapes across species and modeled conditions that represented historical and contemporary mechanisms. The characteristics of genomic landscapes differed across species, influenced by varying levels of population structuring and admixture between deserts, and the best-fit models contrasted between the whole genome and partitions along the genome. Both historical and contemporary mechanisms were important in explaining genetic distance, but particularly past and current environments, suggesting that genomic evolution was modulated by climate and habitat There were also different best-ftit models across genomic partitions of the data, indicating that these regions capture different evolutionary histories. These results show that the genomic landscape of differentiation can be associated with alternative geographic factors operating on different portions of the genome, which reflect how heterogeneous patterns of genetic differentiationmore »can evolve across species and genomes.

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