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bioRxiv · 10.64898/2026.01.27.702068

The tortured past of young polymorphic sex chromosomes revealed through multiple de novo genome assemblies of the mountain pine beetle

Lagunas-Robles, G.·Bentz, B.·Verma, M.·Vandygriff, J.·Hansen, M.·Simmonds, T.·Corpuz, R.·Kauwe, A.·Geib, S.·Bracewell, R. R.
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Abstract

Neo-sex chromosomes provide a powerful system for studying the early stages of sex chromosome evolution and the genomic mechanisms that may contribute to reproductive isolation. Using PacBio long-read HiFi sequencing, Hi-C scaffolding, and sex-specific transcriptomic data, we generated six chromosome-level assemblies (male and female from three populations) of the mountain pine beetle (Dendroctonus ponderosae), a species known to harbor three partially reproductively isolated neo-Y haplogroups. These assemblies reveal that the large neo-X and neo-Y chromosomes formed through sequential fusions of the ancestral X with three autosomes, with recombination cessation occurring at [~]8.6, [~]6.3, and [~]4.3 MYA for each event. Comparative analyses show that while neo-X chromosomes remain largely collinear across populations, neo-Ys exhibit dramatic structural divergence, with 900-1,200 inverted segments per haplogroup and only [~]65% of sequence able to be aligned to the neo-X. Repeat analyses demonstrate moderate TE accumulation on the neo-Y, particularly LTR elements, and gene mapping analyses reveal extensive degeneration: [~]62% of neo-Y genes exhibit gene loss, fragmentation, or disruptive mutations. All populations retain a single pseudoautosomal region (PAR), though PAR size and gene content vary due to neo-Y specific rearrangements. Across neo-Ys, 27 genes are uniquely missing in the Western haplogroup, including previously identified candidates implicated in hybrid male sterility. Broader comparisons among neo-Ys show widespread structural variation, population specific patterns of degeneration, and limited gene family expansions. Together, these results provide the first full characterization of neo-sex chromosome evolution in D. ponderosae, revealing rapid, lineage specific neo-Y degeneration and highlighting the potential for sex chromosome divergence to contribute to emerging reproductive incompatibilities within a single species.

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Lagunas-Robles, G., Bentz, B., Verma, M., Vandygriff, J., Hansen, M., Simmonds, T., Corpuz, R., Kauwe, A., Geib, S., Bracewell, R. R.. 2026-01-30. The tortured past of young polymorphic sex chromosomes revealed through multiple de novo genome assemblies of the mountain pine beetle. https://doi.org/10.64898/2026.01.27.702068

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