The Evolutionary Genomics of Serpentine Adaptation

Serpentine barrens are among the most challenging settings for plant life. Representing a perfect storm of hazards, serpentines consist of broadly skewed elemental profiles, including abundant toxic metals and low nutrient contents on drought-prone, patchily distributed substrates. Accordingly, plants that can tolerate the challenges of serpentine have fascinated biologists for decades, yielding important insights into adaptation to novel ecologies through physiological change. Here we highlight recent progress from studies which demonstrate the power of serpentine as a model for the genomics of adaptation. Given the moderate – but still tractable – complexity presented by the mix of hazards on serpentine, these venues are well-suited for the experimental inquiry of adaptation both in natural and manipulated conditions. Moreover, the island-like distribution of serpentines across landscapes provides abundant natural replicates, offering power to evolutionary genomic inference. Exciting recent insights into the genomic basis of serpentine adaptation point to a partly shared basis that involves sampling from common allele pools available from retained ancestral polymorphism or via gene flow. However, a lack of integrated studies deconstructing complex adaptations and linking candidate alleles with fitness consequences leaves room for much deeper exploration. Thus, we still seek the crucial direct link between the phenotypic effect of candidate alleles and their measured adaptive value – a prize that is exceedingly rare to achieve in any study of adaptation. We expect that closing this gap is not far off using the promising model systems described here.

Deep Convergence, Shared Ancestry, and Evolutionary Novelty in the Genetic Architecture of Heliconius Mimicry

Convergent evolution can occur through different genetic mechanisms in different species. It is now clear that convergence at the genetic level is also widespread, and can be caused by either (i) parallel genetic evolution, where independently evolved convergent mutations arise in different populations or species, or (ii) collateral evolution in which shared ancestry results from either ancestral polymorphism or introgression among taxa. The adaptive radiation of Heliconius butterflies shows color pattern variation within species, as well as mimetic convergence between species. Using comparisons from across multiple hybrid zones, we use signals of shared ancestry to identify and refine multiple putative regulatory elements in Heliconius melpomene and its comimics, Heliconius elevatus and Heliconius besckei, around three known major color patterning genes: optix, WntA, and cortex. While we find that convergence between H. melpomene and H. elevatus is caused by a complex history of collateral evolution via introgression in the Amazon, convergence between these species in the Guianas appears to have evolved independently. Thus, we find adaptive convergent genetic evolution to be a key driver of regulatory changes that lead to rapid phenotypic changes. Furthermore, we uncover evidence of parallel genetic evolution at some loci around optix and WntA in H. melpomene and its distant comimic Heliconius erato. Ultimately, we show that all three of convergence, conservation, and novelty underlie the modular architecture of Heliconius color pattern mimicry.

A shared genetic basis of mimicry across swallowtail butterflies points to ancestral co-option of doublesex

Uncovering whether convergent adaptations share a genetic basis is consequential for understanding the evolution of phenotypic diversity. This information can help us understand the extent to which shared ancestry or independent evolution shape adaptive phenotypes. In this study, we first ask whether the same genes underlie polymorphic mimicry in Papilio swallowtail butterflies. By comparing signatures of genetic variation between polymorphic and monomorphic species, we then investigate how ancestral variation, hybridization, and independent evolution contributed to wing pattern diversity in this group. We report that a single gene, doublesex (dsx), controls mimicry across multiple taxa, but with species-specific patterns of genetic differentiation and linkage disequilibrium. In contrast to widespread examples of phenotypic evolution driven by introgression, our analyses reveal distinct mimicry alleles. We conclude that mimicry evolution in this group was likely facilitated by ancestral polymorphism resulting from early co-option of dsx as a mimicry locus, and that evolutionary turnover of dsx alleles may underlie the wing pattern diversity of extant polymorphic and monomorphic lineages.

Inversions shape the divergence of Drosophila pseudoobscura and D. persimilis on multiple timescales

By shaping meiotic recombination, chromosomal inversions can influence genetic exchange between hybridizing species. Despite the recognized importance of inversions in evolutionary processes such as divergence and speciation, teasing apart the effects of inversions over time remains challenging. For example, are their effects on sequence divergence primarily generated through creating blocks of linkage-disequilibrium pre-speciation or through preventing gene flux after speciation? We provide a comprehensive look into the influence of chromosomal inversions on gene flow throughout the evolutionary history of a classic system: Drosophila pseudoobscura and D. persimilis. We use extensive whole-genome sequence data to report patterns of introgression and divergence with respect to chromosomal arrangements. Overall, we find evidence that inversions have contributed to divergence patterns between Drosophila pseudoobscura and D. persimilis over three distinct timescales: 1) pre-speciation segregation of ancestral polymorphism, 2) post-speciation ancient gene flow, and 3) recent gene flow. We discuss these results in terms of our understanding of evolution in this classic system and provide cautions for interpreting divergence measures in similar datasets in other systems.

Genetic variability of populations of the white-eared opossum, Didelphis albiventris Lund 1840 (Didelphimorphia; Didelphidae) in Brazil

Didelphis albiventris are found throughout Northeast and Central Brazil to central-southern Uruguay and it was subject of few studies in a population level. Given this, the present study investigated the genetic variability of the species using the mitochondrial molecular marker cytochrome oxidase c subunit I. We analyzed samples from the different biomes within three Brazilian regions: Northeast (Caatinga , Cerrado, and Atlantic Forest), Southeast (Cerrado , Atlantic Forest, Cerrado/Atlantic Forest, and Cerrado/Caatinga ecotones) and South (Pampa and Atlantic Forest). Software BAPs retrieved five distinct demes: dm 1, dm 2, and dm 5 that occurs in South, Northeast and Southeast regions respectively and the dm 3 and dm 4 are wide distributed in Northeast and Southeast. Population analysis performed with AMOVA, haplotype network and Mantel test estimated the veracity of the demes. The FST shows structuring for the five demes, with dm 1 (South region) isolated from the others, however the other analysis showed the Northeast/Southeast demes (dm 2-5) united, diagnosing gene flow between them, mainly at the transitional zones, in areas as far away as areas with similar latitude interval (Southeast vs South) that was not detected gene flow. In the haplotype network, the mutational steps was conclusive in split dm1 from dm 2-5 with 15 mutational steps and the Mantel test was moderated, which is explained by genetic similarity despite the great geographic distances (Northeast/Southeast). Thus, our analysis recognized two different lineages (South and Northeast/Southeast) and indicate that the biomes were not decisive in their isolation. The sharing of demes at the transitional zones and in areas with high latitudinal intervals reflects a recent ancestral polymorphism for D. albiventris. The plasticity in the occupation of the space by this species contributes in its wide dispersion capability, that is, geographical distribution. Our results revealed important implications for the management of D. albiventris in these transitional zones areas where demes were shared.

Polymorphisms and distribution of South American manatees (Trichechus spp.)

Traditionally, the morphological attributes and the range of Trichechus species have been clearly established. However, we herein show that morphological traits, like belly and pectoral flipper coloration in South American manatees may be polymorphic. Karyotypic analysis of T. manatus allowed the precise identification of this species and confirmed the variability of the observed morphological findings. Molecular analysis based on cytochrome b DNA and the D-loop mitochondrial region showed shared haplotypes between T. inunguis and T. manatus, suggesting the presence of an ancestral polymorphism. These findings showed the need of improving the identification of these species before implementing conservation strategies. Finally, we present a complete report on the extant distribution of these species in South America.

Genealogy in evolution

Chapter 5, “Genealogy in evolution,” introduces branching tree diagrams as an intuitive way to visualize the evolutionary relationships between alleles, haplotypes, individuals, and species. It describes the nomenclature of gene tree topologies, the stochasticity in tree shape across genes, and the notion of a most recent common ancestor. This chapter also covers reverse-time genealogical thinking with coalescent theory and how it integrates with predictions about nucleotide polymorphism and the site frequency spectrum. An overview of how phylogenies show between-species genealogical relationships is used to highlight the concepts of orthology and homoplasy, how to calculate and interpret different metrics of DNA sequence divergence, the role of ancestral polymorphism in creating distinct gene trees, the multiple mutational hits problem, and factors that influence calculations of the time to the most recent common ancestor for species trees versus gene trees. This chapter surveys how to think of evolution in terms of genealogies that relate gene copies within a species or among species, and how to connect ideas about gene trees to other ideas in molecular population genetics.

Molecular deviants

Chapter 8, “Molecular deviants: sequence signatures of selection and demography,” dives into the logic and mechanics of some of the most common tests of neutrality to show how and why data can reveal differences from the predictions of the standard neutral model. It introduces approaches based on skewed patterns of polymorphism alone, including Tajima’s D test, and on differentiation or divergence alone, like the Lewontin-Krakauer, Population Branch Statistic (PBS), and K A / K S relative-rates tests. Chapter 8 also covers tests of neutrality that integrate information from both within and between species, including the HKA-test and McDonald-Kreitman (MK) test. The logic for other tests of neutrality also is introduced, including ABBA-BABA, Composite Likelihood Ratio (CLR), Extended Haplotype Homozygosity (EHH), and other approaches. Practical implications of ancestral polymorphism and slightly deleterious polymorphisms are discussed, for example, in calculating and interpreting the neutrality index and fraction of positively selected sites (α‎). The goal of this chapter is to explain the logic of methods applied to molecular population genetic data to read the story of evolutionary history from the genome.

Polymorphisms and distribution of South American manatees (Trichechus spp.)

Traditionally, the morphological attributes and the range of Trichechus species have been clearly established. However, we herein show that morphological traits, like belly and pectoral flipper coloration in South American manatees may be polymorphic. Karyotypic analysis of T. manatus allowed the precise identification of this species and confirmed the variability of the observed morphological findings. Molecular analysis based on cytochrome b DNA and the D-loop mitochondrial region showed shared haplotypes between T. inunguis and T. manatus, suggesting the presence of an ancestral polymorphism. These findings showed the need of improving the identification of these species before implementing conservation strategies. Finally, we present a complete report on the extant distribution of these species in South America.