Neo-sex Chromosomes in the Monarch Butterfly, Danaus plexippus

Abstract

We report the discovery of a neo-sex chromosome in the monarch butterfly, Danaus plexippus, and several of its close relatives. Z-linked scaffolds in the D. plexippus genome assembly were identified via sex-specific differences in Illumina sequencing coverage. Additionally, a majority of the D. plexippus genome assembly was assigned to chromosomes based on counts of one-to-one orthologs relative to the butterfly Melitaea cinxia (with replication using two other lepidopteran species), in which genome scaffolds have been mapped to linkage groups. Sequencing coverage-based assessments of Z linkage combined with homology-based chromosomal assignments provided strong evidence for a Z-autosome fusion in the Danaus lineage, involving the autosome homologous to chromosome 21 in M. cinxia. Coverage analysis also identified three notable assembly errors resulting in chimeric Z-autosome scaffolds. Cytogenetic analysis further revealed a large W chromosome that is partially euchromatic, consistent with being a neo-W chromosome. The discovery of a neo-Z and the provisional assignment of chromosome linkage for >90% of D. plexippus genes lays the foundation for novel insights concerning sex chromosome evolution in this female-heterogametic model species for functional and evolutionary genomics.

Whole-chromosome hitchhiking driven by a male-killing endosymbiont

“…Although these genomes are diverged by approximately 90 million years, this homology-based approach has been shown previously to be successful for reconstruct chromosomes in a fragmented D. plexippus genome [9]. In total, 282 Mb (87% of the genome) could be confidently assigned to chromosomes (S1 Fig).…”

“…We assembled a high quality draft genome for D. chrysippus, with a total length of 322 Megabases (Mb), a scaffold N50 length of 0.63 Mb, and a BUSCO [28] completeness score of 94% (S1 Table-S8 Table). We then further scaffolded the genome into a pseudo-chromosomal assembly based on homology with the Heliconius melpomene genome [29][30][31] accounting for known fusions that differentiate these species [9,30,32] (Fig. S1).…”

“…A fusion of chromosome 21 to the ancestral Z chromosome occurred in an ancestor of all Danaus species, producing a neo-Z [9,32,54]. It is speculated that a complementary fusion of chromosome 21 to the ancestral W also occurred [9,54], but this is difficult to conclusively verify due to degradation of the W chromosome over longer timescales. If this hypothesis of an ancient neo-W is correct, then the neo-W we describe (W-chr15) might in fact be better described as a neo-neo-W (W-chr21-chr15).…”

“…Although we currently lack linkage information for further scaffolding, we generated a pseudo-chromosomal assembly based on homology with the highly contiguous Heliconius melpomene genome [30,31,65], adjusted for known karyotypic differences [9,[30][31][32]54].…”

“…These contrasting benefits and costs of recombination suppression are of particular interest in the evolution of neo-sex chromosomes, which can form through fusion of autosomes to existing sex chromosomes. There is accumulating evidence that neo-sex chromosomes are common in animals [9][10][11][12][13][14][15], but the processes underlying their emergence, spread and subsequent evolution have not been widely studied. In particular, there are few studied examples of recently-formed neo-sex chromosomes that are not yet fixed in a species.…”