ZZ Top: faster and more adaptive Z chromosome evolution in two Lepidoptera

Abstract

10The rate of divergence for Z or X chromosomes is theoretically predicted to be greater than autosomes, 11 but the possible explanations for this pattern vary, as do empirical results from diverse taxa. Even 12 among moths and butterflies (Lepidoptera), which generally share a single-origin Z chromosome, the 13 handful of available studies give mixed support for faster or more adaptive evolution of the Z 14 chromosome, depending on the species assayed. Here, we examine the molecular evolution of Z 15 chromosomes in two additional lepidopteran species: the Carolina sphinx moth and the monarch 16 butterfly, the latter of which possesses a recent chromosomal fusion yielding a segment of newly Z-17 linked DNA. We find evidence for both faster and more adaptive Z chromosome evolution in both 18 species, though this effect is strongest in the neo-Z portion of the monarch sex chromosome. The neo-Z 19 is less male-biased than expected of a Z chromosome, and unbiased and female-biased genes drive the 20 signal for adaptive evolution here. Together these results suggest that male-biased gene accumulation 21 and haploid selection have opposing effects on long-term rates of adaptation and may help explain the 22 discrepancies in previous findings as well as the repeated evolution of neo-sex chromosomes in 23Lepidoptera. 24 388 This project was funded by the NSF DDIG (DEB-1701931). The authors wish to acknowledge Wesley 389Mason and Michael Hulet and the rest of the Information and Telecommunication Technology Center 390 (ITTC) staff at the University of Kansas for their support with our high-performance computing. We are 391 continually grateful to Chip Taylor and Ann Ryan from MonarchWatch for access to butterflies and to 392 Clyde Sorenson for logistical and moral support in obtaining sphinx moths. Thanks, as well, to Alex 393Mackintosh and other frequenters of the Darwin Dance Hall for conversations during the interpretation 394 of these results. 395

Population differentiation and structural variation in theManduca sextagenome across the United States

“…Additionally, although synteny is generally well-conserved between Manduca and Bombyx , some regions have diverged enough between species that they could not be placed on scaffolds via synteny-approaches. For Z-linked regions, we could recover linkage of non-syntenic scaffolds based on male-to-female coverage differences (Mongue et al, 2020) but for autosomal scaffolds, these sequences remain unplaced for the time being.…”

“…unbiased genes), compared to the rest of the Z chromosome, which is male-biased (Mongue & Walters, 2017). As has been recently shown, unbiased genes are an important source of positive selection on the Z in M. sexta (Mongue et al, 2020). These genes are expressed in a haploid state in females (which have only one Z chromosome); thus, even recessive mutations are exposed to selection (Charlesworth, Coyne, & Barton, 1987;Rice, 1984).…”

“…All pairwise comparisons were performed: North Carolina (NC) – Arizona (AZ), Kansas (KS) – Arizona, and NC – KS. For these analyses, published chromosome assignments of scaffolds were employed (Kanost et al, 2016; Mongue, Hansen, & Walters, 2020; Mongue & Walters, 2017). Importantly, these assignments, which used a mixture of synteny (i.e conserved ordering of orthologous genes) and sex-differences in coverage (to identify the Z chromosome), did not contain information on ordering of scaffolds within a chromosome.…”

“…For these analyses, published chromosome assignments of scaffolds were employed for the older assembly (Kanost et al . 2016; Mongue and Walters 2017; Mongue et al . 2020) and assignments generated for this manuscript were used for the new assembly.…”

“…Manduca sexta has a wealth of available RNA sequence data from both sexes and different life-stages, aggregated as a set of RNAseq collected by Cao and Jiang (2017) and quantified with this older reference. From this dataset, the specificity of gene expression was calculated for each gene in the genome for life-stage, tissue, and sex-specificity (following methods in Mongue, Hansen, & Walters, 2020) to inform potential function of genes-of-interest. More precisely, the specificity metric (SPM) was used to assess the proportion of a given gene’s expression found in a specific class.…”