Fitness consequences of polymorphic inversions in the zebra finch genome

Abstract

BackgroundInversion polymorphisms constitute an evolutionary puzzle: they should increase embryo mortality in heterokaryotypic individuals but still they are widespread in some taxa. Some insect species have evolved mechanisms to reduce the cost of embryo mortality but humans have not. In birds, a detailed analysis is missing although intraspecific inversion polymorphisms are regarded as common. In Australian zebra finches (Taeniopygia guttata), two polymorphic inversions are known cytogenetically and we set out to detect these two and potentially additional inversions using genomic tools and study their effects on embryo mortality and other fitness-related and morphological traits.ResultsUsing whole-genome SNP data, we screened 948 wild zebra finches for polymorphic inversions and describe four large (12–63 Mb) intraspecific inversion polymorphisms with allele frequencies close to 50 %. Using additional data from 5229 birds and 9764 eggs from wild and three captive zebra finch populations, we show that only the largest inversions increase embryo mortality in heterokaryotypic males, with surprisingly small effect sizes. We test for a heterozygote advantage on other fitness components but find no evidence for heterosis for any of the inversions. Yet, we find strong additive effects on several morphological traits.ConclusionsThe mechanism that has carried the derived inversion haplotypes to such high allele frequencies remains elusive. It appears that selection has effectively minimized the costs associated with inversions in zebra finches. The highly skewed distribution of recombination events towards the chromosome ends in zebra finches and other estrildid species may function to minimize crossovers in the inverted regions.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1056-3) contains supplementary material, which is available to authorized users.

Evolution of bird genomes—a transposon's‐eye view

“…), as well as three contig‐level assemblies (Table S1, online only). Another way to assess the quality of a genome assembly is to look at the representation of highly similar repetitive regions (e.g., very young TE insertions), which are difficult to assemble . As mentioned above, short‐read genome assemblies consistently underestimate the amount of very recent TE‐derived DNA (Fig.…”

“…Yet, it is worth noting that the zebra finch lineage underwent high amounts of intrachromosomal rearrangements, such as inversions . Recent studies involving up to 21 bird genome assemblies suggest additional evidence for frequent interchromosomal and intrachromosomal rearrangements during bird evolution .…”

Association mapping of morphological traits in wild and captive zebra finches: reliable within, but not between populations

“… SNPs in DKK3 on chromosome Tgu5_random are linked to a polymorphic inversion on chromosome Tgu5 , which extends from around 0.9–15 Mb (Knief et al . ). QTL peaks on chromosome Tgu5 span almost the entire chromosome, starting at the first SNP in our linkage map.…”

“…We also included 41 SNPs genotyped in the validation sample for a different purpose (described in Knief et al . ).…”

“…An FDR of 0.5 is admittedly high, but we expected a priori many associations to be true because the SNPs reside in previously identified QTL regions (Sham & Purcell 2014). We also included 41 SNPs genotyped in the validation sample for a different purpose (described in Knief et al 2016).…”