A Chromosome-Level Reference Genome for the Black-Legged Kittiwake (Rissa tridactyla), a Declining Circumpolar Seabird

Abstract

Amidst the current biodiversity crisis, the availability of genomic resources for declining species can provide important insights into the factors driving population decline. In the early 1990s, the black-legged kittiwake (Rissa tridactyla), a pelagic gull widely distributed across the arctic, subarctic, and temperate zones, suffered a steep population decline following an abrupt warming of sea surface temperature across its distribution range and is currently listed as Vulnerable by the International Union for the Conservation of Nature. Kittiwakes have long been the focus for field studies of physiology, ecology, and ecotoxicology and are primary indicators of fluctuating ecological conditions in arctic and subarctic marine ecosystems. We present a high-quality chromosome-level reference genome and annotation for the black-legged kittiwake using a combination of Pacific Biosciences HiFi sequencing, Bionano optical maps, Hi-C reads, and RNA-Seq data. The final assembly spans 1.35 Gb across 32 chromosomes, with a scaffold N50 of 88.21 Mb and a BUSCO completeness of 97.4%. This genome assembly substantially improves the quality of a previous draft genome, showing an approximately 5× increase in contiguity and a more complete annotation. Using this new chromosome-level reference genome and three more chromosome-level assemblies of Charadriiformes, we uncover several lineage-specific chromosome fusions and fissions, but find no shared rearrangements, suggesting that interchromosomal rearrangements have been commonplace throughout the diversification of Charadriiformes. This new high-quality genome assembly will enable population genomic, transcriptomic, and phenotype-genotype association studies in a widely studied sentinel species, which may provide important insights into the impacts of global change on marine systems.

Keywords: Arctic; Charadriiformes; chromosomal rearrangements; chromosome-level genome assembly; gull; population decline.

Fig. 1.

A chromosome-level genome assembly for the black-legged kittiwake (bRisTri1) and interchromosomal rearrangements across Charadriiformes. (a) Alignment of bRisTri1 and OUT-0021 genome assemblies. For each chromosome, the bottom track represents the regions of bRisTri1 chromosomes that aligned (peach) or did not align (violet) to a sequence of the OUT-0021 assembly. The middle track represents the repeat content in windows of 1 kbp, with darker green representing higher repeat content as shown in the legend. The top track shows the assembly gaps as black bars. (b) Raincloud plots showing the GC content in aligned and nonaligned regions between the two assemblies. (c) Repeat content in the same regions. (d) Hap-mer blob plot of the bRisTri assembly. Each blob represents a contig, and its size is proportional to contig size. Red blobs represent maternal haplotype contigs, whereas blue blobs represent paternal haplotype contigs. Each blob is plotted according to the number of paternal and maternal hap-mers that it contains. The fact that there are very few paternal-specific k-mers in the maternal assembly and vice versa suggests that each contig was successfully phased. (e) Pairwise whole-genome alignments across four chromosome-level Charadriiformes genomes (black-legged kittiwake, common tern, razorbill, and European golden plover) and two outgroups (zebra finch and chicken). Horizontal bars represent chromosomes and are colored in green for the Charadriiformes, turquoise for the zebra finch, and purple for the chicken. Chromosomes are ordered by the chicken chromosome IDs, which are labeled at the bottom of the figure. Black-legged kittiwake chromosome IDs for chromosomes that have experienced interchromosomal rearrangements in the Charadriiformes are labeled at the top, and these chromosomes are highlighted in colors. Bird illustrations reproduced with permission by Lynx Edicions.