Chromosomal rearrangements preserve adaptive divergence in ecological speciation

Despite increasing empirical evidence that chromosomal rearrangements may play an important role in adaptive divergence and speciation, the degree to which divergent genomic regions are associated with chromosomal rearrangements remains unclear. In this study, we provide the first whole-genome analyses of ecological speciation and chromosomal evolution in a Daphnia species complex, using chromosome-scale assemblies and natural-population sequencing of the recently diverged species pair, Daphnia pulicaria and Daphnia pulex, which occupy distinct yet overlapping habitats in North America, and the outgroup species Daphnia obtusa. Our results describe a mixed mode of geographic divergence (isolation with secondary contact) resulting in a heterogeneous landscape of genomic divergence. Large contiguous continents of divergence encompass over one third of the genome (36%) and contain nearly all the fixed differences (94%) between the species, while the background genome has been homogenized. Chromosomal rearrangements between species, including inversions and intrachromosomal translocations, are associated with the continents of divergence and capture multiple adaptive alleles in genes and pathways thought to contribute to the species phenotypic differences.

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dbVar structural variant cluster set for data analysis and variant comparison

F1000Research ◽

10.12688/f1000research.8290.1 ◽

2016 ◽

Vol 5 ◽

pp. 673 ◽

Cited By ~ 10

Author(s):

Lon Phan ◽

Jeffrey Hsu ◽

Le Quang Minh Tri ◽

Michaela Willi ◽

Tamer Mansour ◽

...

Keyword(s):

Genomic Sequence ◽

Chromosomal Rearrangements ◽

Copy Number Variations ◽

Structural Variant ◽

Variant Type ◽

External Data ◽

Cluster Set ◽

Genomic Location ◽

Complex Chromosomal Rearrangements ◽

Genomic Regions

dbVar houses over 3 million submitted structural variants (SSV) from 120 human studies including copy number variations (CNV), insertions, deletions, inversions, translocations, and complex chromosomal rearrangements. Users can submit multiple SSVs to dbVAR that are presumably identical, but were ascertained by different platforms and samples, to calculate whether the variant is rare or common in the population and allow for cross validation. However, because SSV genomic location reporting can vary – including fuzzy locations where the start and/or end points are not precisely known – analysis, comparison, annotation, and reporting of SSVs across studies can be difficult. This project was initiated by the Structural Variant Comparison Group for the purpose of generating a non-redundant set of genomic regions defined by counts of concordance for all human SSVs placed on RefSeq assembly GRCh38 (RefSeq accession GCF_000001405.26). We intend that the availability of these regions, called structural variant clusters (SVCs), will facilitate the analysis, annotation, and exchange of SV data and allow for simplified display in genomic sequence viewers for improved variant interpretation. Sets of SVCs were generated by variant type for each of the 120 studies as well as for a combined set across all studies. Starting from 3.64 million SSVs, 2.5 million and 3.4 million non-redundant SVCs with count >=1 were generated by variant type for each study and across all studies, respectively. In addition, we have developed utilities for annotating, searching, and filtering SVC data in GVF format for computing summary statistics, exporting data for genomic viewers, and annotating the SVC using external data sources.

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Population genomics of parallel hybrid zones in the mimetic butterflies, H. melpomene and H. erato

10.1101/000208 ◽

2013 ◽

Author(s):

Nicola Nadeau ◽

Mayte Ruiz ◽

Patricio Salazar ◽

Brian Counterman ◽

Jose Alejandro Medina ◽

...

Keyword(s):

Population Genomics ◽

De Novo ◽

Reference Sequence ◽

Colour Pattern ◽

Adaptive Divergence ◽

Population Divergence ◽

Hybrid Zones ◽

Data Alignment ◽

Parallel Hybrid ◽

Genomic Regions

Hybrid zones can be valuable tools for studying evolution and identifying genomic regions responsible for adaptive divergence and underlying phenotypic variation. Hybrid zones between subspecies of Heliconius butterflies can be very narrow and are maintained by strong selection acting on colour pattern. The co-mimetic species H. erato and H. melpomene have parallel hybrid zones where both species undergo a change from one colour pattern form to another. We use restriction associated DNA sequencing to obtain several thousand genome wide sequence markers and use these to analyse patterns of population divergence across two pairs of parallel hybrid zones in Peru and Ecuador. We compare two approaches for analysis of this type of data; alignment to a reference genome and de novo assembly, and find that alignment gives the best results for species both closely (H. melpomene) and distantly (H. erato, ~15% divergent) related to the reference sequence. Our results confirm that the colour pattern controlling loci account for the majority of divergent regions across the genome, but we also detect other divergent regions apparently unlinked to colour pattern differences. We also use association mapping to identify previously unmapped colour pattern loci, in particular the Ro locus. Finally, we identify within our sample a new cryptic population of H. timareta in Ecuador, which occurs at relatively low altitude and is mimetic with H. melpomene malleti.

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Tadpoles of hybridising fire-bellied toads (B. bombina and B. variegata) differ in their susceptibility to predation

PLoS ONE ◽

10.1371/journal.pone.0231804 ◽

2020 ◽

Vol 15 (12) ◽

pp. e0231804

Author(s):

Radovan Smolinský ◽

Vojtech Baláž ◽

Beate Nürnberger

Keyword(s):

Direct Evidence ◽

Adaptive Divergence ◽

Differential Adaptation ◽

Risk Of Predation ◽

Distribution Ranges ◽

Bombina Bombina ◽

Recent Debate ◽

The Subject ◽

Genomic Regions

The role of adaptive divergence in the formation of new species has been the subject of much recent debate. The most direct evidence comes from traits that can be shown to have diverged under natural selection and that now contribute to reproductive isolation. Here, we investigate differential adaptation of two fire-bellied toads (Anura, Bombinatoridae) to two types of aquatic habitat. Bombina bombina and B. variegata are two anciently diverged taxa that now reproduce in predator-rich ponds and ephemeral aquatic sites, respectively. Nevertheless, they hybridise extensively wherever their distribution ranges adjoin. We show in laboratory experiments that, as expected, B. variegata tadpoles are at relatively greater risk of predation from dragonfly larvae, even when they display a predator-induced phenotype. These tadpoles spent relatively more time swimming and so prompted more attacks from the visually hunting predators. We argue in the discussion that genomic regions linked to high activity in B. variegata should be barred from introgression into the B. bombina gene pool and thus contribute to gene flow barriers that keep the two taxa from merging into one.

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Phenotypic clines across an unstudied hybrid zone in Woodhouse’s Scrub-Jay (Aphelocoma woodhouseii)

The Auk ◽

10.1093/auk/uky018 ◽

2019 ◽

Vol 136 (2) ◽

Author(s):

Devon A DeRaad ◽

James M Maley ◽

Whitney L E Tsai ◽

John E McCormack

Keyword(s):

Body Size ◽

Contact Zone ◽

Mexico City ◽

Rocky Mountains ◽

Secondary Contact ◽

Genetic Isolation ◽

Southern Mexico ◽

Phenotypic Differences ◽

Northern Mexico ◽

Group A

Abstract Woodhouse’s Scrub-Jay (Aphelocoma woodhouseii) comprises 7 subspecies, ranging from the Rocky Mountains to southern Mexico. We quantified the phenotype of specimens throughout Mexico and found support for significant phenotypic differences between “Sumichrast’s group” in southern Mexico (A. w. sumichrasti and A. w. remota) and the 2 subspecies in northern Mexico, or “Woodhouse’s group” (A. w. grisea and A. w. cyanotis). Despite significant differentiation in body size and mantle color, we found no clear geographic boundary between the groups, suggesting either a geographic cline or hybridization upon secondary contact. We tested for selection against hybridization by fitting models to geographic clines for both body size and back color, and found support for a stable contact zone centered near Mexico City, with selection against intermediate back color. Based on these results, we infer that Sumichrast’s and Woodhouse’s groups diverged during a period of geographic and genetic isolation. The phenotypic introgression between Sumichrast’s and Woodhouse’s groups near Mexico City likely represents a case of recent secondary contact, with selection against hybridization maintaining a geographically stable contact zone.

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Chromosomal Evolution in the Lizard Genus Varanus (Reptilia)

Australian Journal of Biological Sciences ◽

10.1071/bi9750089 ◽

1975 ◽

Vol 28 (1) ◽

pp. 89 ◽

Cited By ~ 31

Author(s):

Max Kinga ◽

Dennis King

Keyword(s):

Chromosome Number ◽

Pericentric Inversion ◽

Sex Chromosome ◽

Chromosomal Rearrangements ◽

Chromosomal Evolution ◽

Size Groups ◽

Sex Chromosome System

The karyotypes have been determined of 16 of the 32 species of the genus Varanus, including animals from Africa, Israel, Malaya and Australia. A constant chromosome number of 2n = 40 was observed. The karyotype is divided into eight pairs of large chromosomes and 12 pairs of microchromosomes. A series of chromosomal rearrangements have become established in both size groups of the karyotype and are restricted to centromere shifts, probably caused by pericentric inversion. Species could be placed in one of six distinct karyotype groups which are differentiated by these rearrangements and whose grouping does not always correspond with the current taxonomy. An unusual sex chromosome system of the ZZjZW type was present in a number of the species examined.

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Extraordinary and extensive karyotypic variation: A 48-fold range in chromosome number in the gall-inducing scale insect Apiomorpha (Hemiptera: Coccoidea: Eriococcidae)

Genome ◽

10.1139/g99-121 ◽

2000 ◽

Vol 43 (2) ◽

pp. 255-263 ◽

Cited By ~ 14

Author(s):

Lyn G Cook

Keyword(s):

Chromosome Number ◽

Chromosomal Rearrangements ◽

Chromosomal Polymorphism ◽

Chromosomal Evolution ◽

Scale Insect ◽

Closely Related Species ◽

Host Genus ◽

Species Complexes ◽

Species Groups ◽

Karyotypic Variation

Chromosome number reflects strong constraints on karyotype evolution, unescaped by the majority of animal taxa. Although there is commonly chromosomal polymorphism among closely related taxa, very large differences in chromosome number are rare. This study reports one of the most extensive chromosomal ranges yet reported for an animal genus. Apiomorpha Rübsaamen (Hemiptera: Coccoidea: Eriococcidae), an endemic Australian gall-inducing scale insect genus, exhibits an extraordinary 48-fold variation in chromosome number with diploid numbers ranging from 4 to about 192. Diploid complements of all other eriococcids examined to date range only from 6 to 28. Closely related species of Apiomorpha usually have very different karyotypes, to the extent that the variation within some species- groups is as great as that across the entire genus. There is extensive chromosomal variation among populations within 17 of the morphologically defined species of Apiomorpha indicating the existence of cryptic species-complexes. The extent and pattern of karyotypic variation suggests rapid chromosomal evolution via fissions and (or) fusions. It is hypothesized that chromosomal rearrangements in Apiomorpha species may be associated with these insects' tracking the radiation of their speciose host genus, Eucalyptus. Key words: Apiomorpha, cytogenetics, chromosomal evolution, holocentric.

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Genome-wide patterns of divergence during speciation: the lake whitefish case study

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2011.0197 ◽

2012 ◽

Vol 367 (1587) ◽

pp. 354-363 ◽

Cited By ~ 81

Author(s):

S. Renaut ◽

N. Maillet ◽

E. Normandeau ◽

C. Sauvage ◽

N. Derome ◽

...

Keyword(s):

Reproductive Isolation ◽

Genomic Islands ◽

Next Generation Sequencing Data ◽

Adaptive Divergence ◽

Phenotypic Traits ◽

Lake Whitefish ◽

Sequencing Data ◽

Species Pairs ◽

Selective Forces ◽

Genomic Regions

The nature, size and distribution of the genomic regions underlying divergence and promoting reproductive isolation remain largely unknown. Here, we summarize ongoing efforts using young (12 000 yr BP) species pairs of lake whitefish ( Coregonus clupeaformis ) to expand our understanding of the initial genomic patterns of divergence observed during speciation. Our results confirmed the predictions that: (i) on average, phenotypic quantitative trait loci (pQTL) show higher F ST values and are more likely to be outliers (and therefore candidates for being targets of divergent selection) than non-pQTL markers; (ii) large islands of divergence rather than small independent regions under selection characterize the early stages of adaptive divergence of lake whitefish; and (iii) there is a general trend towards an increase in terms of numbers and size of genomic regions of divergence from the least (East L.) to the most differentiated species pair (Cliff L.). This is consistent with previous estimates of reproductive isolation between these species pairs being driven by the same selective forces responsible for environment specialization. Altogether, dwarf and normal whitefish species pairs represent a continuum of both morphological and genomic differentiation contributing to ecological speciation. Admittedly, much progress is still required to more finely map and circumscribe genomic islands of speciation. This will be achieved through the use of next generation sequencing data but also through a better quantification of phenotypic traits moulded by selection as organisms adapt to new environmental conditions.

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Adaptive divergence in brain composition between ecologically distinct incipient species

10.1101/043182 ◽

2016 ◽

Author(s):

Stephen H Montgomery ◽

Richard M Merrill

Keyword(s):

Brain Structure ◽

Spatial Information ◽

Ecological Speciation ◽

Distinct Species ◽

Adaptive Divergence ◽

Species Pair ◽

Incipient Species ◽

Brain Structure And Function ◽

Sensory Structures ◽

And Function

During ecological speciation diverging populations are exposed to contrasting sensory and spatial information that present new behavioral and perceptive challenges. Here, we investigate how brain composition evolves during the early stages of speciation. The incipient species pair, Heliconius erato cyrbia and H. himera, have parapatric ranges across an environmental and altitudinal gradient. Despite continuing gene-flow, these species have divergent ecological, behavioral and physiological traits. We demonstrate that these incipient species also differ significantly in brain composition, especially in the size of sensory structures. H. erato has larger visual components whilst H. himera invests more heavily in olfaction. These differences are not explained by environmentally-induced plasticity, but reflect non-allometric shifts in brain structure. Our results suggest the adaptive evolution of brain structure and function play an important role in facilitating the emergence of ecologically distinct species, and imply that plasticity alone may be insufficient to meet the demands of novel environments.

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Genome-wide selection scans integrated with association mapping reveal mechanisms of physiological adaptation across a salinity gradient in killifish

10.1101/254854 ◽

2018 ◽

Cited By ~ 1

Author(s):

Reid S. Brennan ◽

Timothy M. Healy ◽

Heather J. Bryant ◽

Man Van La ◽

Patricia M. Schulte ◽

...

Keyword(s):

Natural Selection ◽

Salinity Tolerance ◽

Hypoxia Tolerance ◽

Physiological Traits ◽

Adaptive Divergence ◽

Genome Wide ◽

Native Populations ◽

Genomic Regions ◽

Insight Into ◽

Freshwater Environments

AbstractAdaptive divergence between marine and freshwater environments is important in generating phyletic diversity within fishes, but the genetic basis of adaptation to freshwater habitats remains poorly understood. Available approaches to detect adaptive loci include genome scans for selection, but these can be difficult to interpret because of incomplete knowledge of the connection between genotype and phenotype. In contrast, genome wide association studies (GWAS) are powerful tools for linking genotype to phenotype, but offer limited insight into the evolutionary forces shaping variation. Here, we combine GWAS and selection scans to identify loci important in the adaptation of complex physiological traits to freshwater environments. We focused on freshwater (FW)-native and brackish water (BW)-native populations of the Atlantic killifish (Fundulus heteroclitus) as well as a population that is a natural admixture of these two populations. We measured phenotypes for multiple physiological traits that differ between populations and that may contribute to adaptation across osmotic niches (salinity tolerance, hypoxia tolerance, metabolic rate, and body shape) and used a reduced representation approach for genome-wide genotyping. Our results show patterns of population divergence in physiological capabilities that are consistent with local adaptation. Selection scans between BW-native and FW-native populations identified genomic regions that presumably aect fitness between BW and FW environments, while GWAS revealed loci that contribute to variation for each physiological trait. There was substantial overlap in the genomic regions putatively under selection and loci associated with the measured physiological traits, suggesting that these phenotypes are important for adaptive divergence between BW and FW environments. Our analysis also implicates candidate genes likely involved in physiological capabilities, some of which validate a priori hypotheses. Together, these data provide insight into the mechanisms that enable diversification of fishes across osmotic boundaries.Author SummaryIdentifying the genes that underlie adaptation is important for understanding the evolutionary process, but this is technically challenging. We bring multiple lines of evidence to bear for identifying genes that underlie adaptive divergence. Specifically, we integrate genotype-phenotype association mapping with genome-wide scans for signatures of natural selection to reveal genes that underlie phenotypic variation and that are adaptive in populations of killifish that are diverging between marine and freshwater environments. Because adaptation is likely manifest in multiple physiological traits, we focus on hypoxia tolerance, salinity tolerance, and metabolic rate; traits that are divergent between marine and freshwater populations. We show that each of these phenotypes is evolving by natural selection between environments; genetic variants that contribute to variation in these physiological traits tend to be evolving by natural selection between marine and freshwater populations. Furthermore, one of our top candidate genes provides a mechanistic explanation for previous hypotheses that suggest the adaptive importance of cellular tight junctions. Together, these data demonstrate a powerful approach to identify genes involved in adaptation and help to reveal the mechanisms enabling transitions of fishes across osmotic boundaries.

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Genomic signatures of rapid adaptive divergence in a tropical montane species

Biology Letters ◽

10.1098/rsbl.2021.0089 ◽

2021 ◽

Vol 17 (7) ◽

pp. 20210089

Author(s):

Per G. P. Ericson ◽

Martin Irestedt ◽

Huishang She ◽

Yanhua Qu

Keyword(s):

Environmental Heterogeneity ◽

Adaptive Divergence ◽

Glacial Cycles ◽

Genomic Signatures ◽

Tropical Mountain ◽

Population Genomic ◽

Allopatric Divergence ◽

Suitable Habitats ◽

Genomic Regions ◽

Two Populations

Mountain regions contain extraordinary biodiversity. The environmental heterogeneity and glacial cycles often accelerate speciation and adaptation of montane species, but how these processes influence the genomic differentiation of these species is largely unknown. Using a novel chromosome-level genome and population genomic comparisons, we study allopatric divergence and selection in an iconic bird living in a tropical mountain region in New Guinea, Archbold's bowerbird ( Amblyornis papuensis ). Our results show that the two populations inhabiting the eastern and western Central Range became isolated ca 11 800 years ago, probably because the suitable habitats for this cold-tolerating bird decreased when the climate got warmer. Our genomic scans detect that genes in highly divergent genomic regions are over-represented in developmental processes, which is probably associated with the observed differences in body size between the populations. Overall, our results suggest that environmental differences between the eastern and western Central Range probably drive adaptive divergence between them.

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