Neo-sex chromosome characterization and its applications to
studies of chromosomal evolution
Alignment of the draft neo-Y scaffolds to the neo-X revealed the
approximate boundary between the ancestral-autosomal and ancestral-X
portions of the neo-X chromosome. Our data suggest that the ancestral-X
region may be slightly larger than 10 Mb (Fig. 5), or approximately 14%
of the total length of the neo-X chromosome.
Using linkage mapping and genome assemblies, we found that markers in
each of the first four principal components (PCs) identified in Trevoy
et al. (2019) were physically linked to three chromosomes. These
findings validate the use of PC loadings exhibiting marker plateaus to
infer genomic linkage in the absence of a linkage map or
chromosome-scale genome assembly. Trevoy et al. (2019) also showed that
high PC 2 loadings distinguished SNPs in beetles that were almost
entirely heterozygous in males and homozygous in females. They
hypothesized that this reflects sex-specific nucleotide changes in
paralogous neo-X linked versus neo-Y linked genes. If true, the
male-specific heterozygosity found by Trevoy et al. (2019) actually
resulted from erroneous alignment of neo-Y reads to the
ancestral-autosomal region of the neo-X. Support for this conclusion
comes from neo-Y scaffold locations on the draft genome, as identified
by Dowle et al. (2017), mapping to our neo-X chromosome (Fig. 5).
Further, if any of the draft genome scaffolds containing high-loading
SNPs on the PC 2 axis identified by Trevoy et al. (2019) truly
represented the male copy of the neo-X, we would expect some of them to
align to the ancestral-X region as well, but this was not the case.
Rather, we identify a mosaic-like pattern across neo-Y scaffolds that is
consistent with both the recent origin of mountain pine beetle neo-sex
chromosomes and the gradual accumulation of chromosome-specific
mutations.
Karyotype varies across Dendroctonus and includes both typical
Xyp sex chromosomes (as found for the majority of
beetles) and neo-sex chromosomes (Zúñiga et al., 2002), like in mountain
pine beetle. We have generated the first chromosome-level assembly in
this genus, and others are forthcoming (Casola et al., 2020; Keeling et
al., 2020). The mountain pine beetle neo-sex chromosomes represent
approximately 30% of its genome content. Genome assemblies from the
other Dendroctonus spp. should identify which ancestral autosomes
became part of the neo-sex chromosomes in mountain pine beetle, and the
consequences of such large sex chromosomes for mountain pine beetle
physiology and ecology.
This improved mountain pine beetle genome may provide another window for
studying chromosome evolution relating to neo-XY development and Y
chromosome degeneration. Currently, much of our understanding of neo-XY
systems comes from studies of Drosophila spp. (Wei & Bachtrog,
2019), while mammalian and Drosophila systems provide insight
into Y degeneration (e.g., Muller’s ratchet) (Charlesworth &
Charlesworth, 2000). However, neither mammals nor Drosophila are
ideal systems for these studies because divergence times among species
can be considerable – their Y chromosomes tend to be quite old,
exhibiting substantial degeneration (Charlesworth & Charlesworth,
2000). Thus, evolutionarily more recent neo-Y systems, like that of
mountain pine beetle, are particularly valuable.
Several other features of the mountain pine beetle genome, coupled with
the improved genomic resource presented here, make it an interesting
chromosomal evolution study system. First, compared to traditional
chiasmatic or achiasmatic XY systems, the ancestral Xypkaryotypes of many Dendroctonus spp. may more readily result in
neo-XY systems. (Blackmon & Demuth, 2014; Dutrillaux & Dutrillaux,
2017). Second, Y turnover, due to degeneration followed by neo-Y gains,
is common in many beetle groups, and is approximately 34% inDendroctonus (Blackmon & Demuth, 2014). Third, neo-Y haplotype
groups corresponding to geography and low hybrid viability have been
identified in the mountain pine beetle (Dowle et al., 2017). Thus,
further study of the mountain pine beetle genome may allow us to answer
a variety of questions relating to Muller’s ratchet-related concepts,
and implications for neo-Y chromosome turnover, in phylogeographic and
cyclic population irruption contexts.
In conclusion, we completed proximity ligation-based scaffolding of the
draft genome of D. ponderosae , supported by linkage mapping, to
generate chromosome-level assemblies. These assemblies support
genome-level investigations of many biological processes for this
keystone species and silvicultural pest and will serve as a valuable
resource for functional and evolutionary studies of otherDendroctonus species, other Scolytinae and Coleoptera more
generally.