Análisis de resultados del módulo de extremos

Joshua V. Peñalba, Andrew Cockburn, Leo Joseph, Craig Moritz

Abstract

Chromosomal rearrangements have been implicated as important drivers of adaptation and speciation in many species. The increasing availability of reference genome sequences has started to reveal the importance of a particular form of chromosomal rearrangement, inversions, in selection and speciation by reducing recombination between adaptive combinations of alleles. In birds, this has been of particular interest. Other types of rearrangements, such as translocations, are uncommon which provides an explanation for the high synteny of bird genomes. Characterizing the frequency and form of inversions requires chromosome-scale genome assemblies, which remain sparse across birds. To estimate the prevalence of inversions across the bird tree, we complemented existing chromosome-scale

assemblies with a chromosome-scale assembly of the superb fairywren (Malurus

cyaneus) which occupies a distinctive branch of the oscine passerines. Whole chromosome alignments of the macrochromosomes of eight avian genomes show a correlation between the number of inversions and the chromosome size.

Furthermore, the Z chromosome is shown to be particularly rich with inversions relative to autosomes of similar size. Lastly, we show that more chromosomal

inversions are fixed between oscine passerine clades relative to non-passerine clades. This suggests that the dynamics of chromosome rearrangements, and how they may facilitate divergence and speciation, may vary between the oscine passerines, which comprise more than half the world’s bird diversity, and the non-passerines.

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Introduction

Genomic architecture is a major component of variation in genome

divergence. It provides the intrinsic, structural context in which different genomic regions may interact and respond to extrinsic forces such selection, drift, and gene flow. The term “genome architecture” can refer broadly to gene order along

chromosomes, structural variation, and other genomic features such as centromeres, telomeres, or repeat elements. Ultimately, these features influence variation in recombination rate across the genome and consequently nucleotide diversity and divergence (Burri, 2017; Cruickshank & Hahn, 2014; Ravinet et al., 2017). Genomic architecture, then, may govern how selection affects both target genes and physically linked regions and whether gene flow affects small units or large blocks.

Understanding the evolutionary dynamics of different features of genomic

architecture and how they will lead to an improved understanding of the role they play in divergence, adaptation, speciation, and diversification (Potter et al., 2017).

Chromosomal inversions serve as an effective mechanism to reduce recombination in a localized region in the genome, occasionally coinciding with peaks in divergence (Kulathinal, Stevison, & Noor, 2009; Poelstra et al., 2014; Turner, Hahn, & Nuzhdin, 2005). If a chromosomal inversion appears in a population, individuals heterozygous for the inversion would see a localized suppression in recombination as it may disrupt chromosome alignment during meiosis (Kirkpatrick, 2010). If an inversion captures two alleles which are

independently advantageous, selection would increase the frequency of the inversion in a population (Hoffmann & Rieseberg, 2008). Effectively, these inversions can serve as efficient barriers to gene flow if the allelic combinations within them are under differential selection between the two populations (Feder & Nosil, 2009; Hoffmann & Rieseberg, 2008). Although the presence of inversions alone may not immediately serve as barriers to gene flow (Davey et al., 2017; Horn et al., 2012), the combination of inversions and the selective coefficients of alleles that reside within may facilitate divergence between populations with ongoing gene flow.

This reduction in recombination and gene flow underpin the importance of chromosomal inversions in speciation (Ayala, Ullastres, & González, 2014; Jones et al., 2012). Many studies have shown that the presence of inversions is correlated

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with higher divergence or increased speciation rate (Bush, Case, Wilson, & Patton, 1977; Navarro & Barton, 2003b). These inversions can link genes related to mate- preference with those related to ecological selection resulting in what some call ‘supergenes’ (Taylor & Campagna, 2016; Thompson & Jiggins, 2014), although this is a controversial concept because empirical data often only highlight one functional variant associated with the inversion. The importance of inversions in speciation, however, necessitates gene flow between diverging populations as it serves as an intrinsic barrier to populations with limited to no prezygotic isolating mechanisms. Furthermore, epistatic interactions and genomic incompatibilities help select for reduced recombination and may eventually recruit the inversion to facilitate divergence between populations (Kirkpatrick & Barton, 2006; Navarro & Barton, 2003a; Noor, Grams, Bertucci, & Reiland, 2001). A recent model proposed that inversions also may be involved in prezygotic isolation if a mating preference locus is captured with at least one locus involved in epistatic incompatibilities (Dagilis & Kirkpatrick, 2016). This would reduce the cost associated with matings leading to offspring with incompatible alleles. This model may be particularly pertinent in systems where postzygotic reproductive isolation is decoupled from speciation rates, such as in birds (Rabosky & Matute, 2013)

Interest in chromosomal inversions in birds is growing. Recent studies have shown that although the interchromosomal structure has been fairly conserved among birds, intrachromosomal rearrangements have been common (Ellegren, 2010; Hooper & Price, 2015; Nanda, Benisch, Fetting, Haaf, & Schmid, 2011). Chromosomal inversions in birds have been implicated in maintaining phenotypic morphs of hybridizing crows (Poelstra et al., 2014), variation in mating strategies in ruffs (Lamichhaney et al., 2016), and affecting sperm morphology in zebra finches (Kim et al., 2017; Knief et al., 2017). Consistent with the requirement that gene flow is necessary for inversions to be relevant for speciation, sister species of birds with range overlap tend to have higher prevalence of fixed pericentric inversions compared to their allopatric counterparts (Hooper & Price, 2015, 2017). These previous studies have primarily focused on a particular species complex or coarse- scale karyotype data. The growing resources of chromosome-scale reference

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genomes can start to shed light on inversions inferred from sequence data on a broad scale (Damas et al., 2017; Laine et al., 2016; Warren et al., 2010, 2017).

To address this, we leveraged existing chromosome-scale genome assemblies across the avian tree then sequenced and assembled a new chromosome-scale

reference genome of the superb fairywren (Malurus cyaneus). The superb fairywren

is a small, insectivorous bird in the oscine infraorder Meliphagides (Cracraft 2014) which has had no detailed genomic resources published. Found in southeastern Australia, the superb fairywren exhibits strong sexual dimorphism during the breeding season and has been a model system in studying the ecology of cooperative breeding systems (Cockburn et al. 2016). A multi-decade study of the superb

fairywren population located in the Australian National Botanical Gardens,

Canberra provide a well-sampled pedigree which can used to generate a linkage map and thereby assist with chromosome-scale genome assemblies. Existing genomic resources for passerines (Passeriformes) have been limited to species within the infraorder Passerides (Cracraft 2014). By sequencing a species from the Australasian endemic Meliphagides, we fill a phylogenetic gap spanning opposite ends of the

oscine tree (diverged ~30-40 Mya). Complementary to the non-passerine Gallus

gallus (Galliformes), Coturnix japonica (Galliformes), and Columba livia

(Columbiformes) genomes, this set of passerine genomes sample multiple parts of the bird tree providing opportunity for a preliminary comparative study on chromosomal evolution in birds. With this we ask (1) are there chromosomal rearrangements unique to the superb fairywren at this level of sampling? (2) how do chromosomal inversions vary between the macrochromosomes and Z chromosome? and (3) how does the frequency of chromosomal inversions vary between oscine passerines (~47% of all bird species) and non-passerines?

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Figure 1. Phylogeny of bird genomes stored in GenBank (accessed 24 Oct 2017) following (Jetz et al. 2012). Bars represent scaffold N50 from the GenBank assembly quality information. Dark blue bars and illustrations represent available

chromosome-scale genomes while the light blue bars represent scaffold level assemblies. Assembly N50 could represent scaffolds or superscaffolds but the distinction is not currently available. Higher level taxonomy is highlighted in the phylogeny and the superb fairywren is labeled.