Chromosome-length genome assembly of Uta stansburiana and gene expression data reveal fast pace-of-life comes with environmental stability

Abstract

Uta stansburiana are an emerging model system for studying sexual selection, polymorphism, and the evolution of pace-of-life syndromes (POLS) whose distribution covers variable environments and a wide latitudinal gradient. POLS are suites of traits causing variation of life history along a slow maturing-fast maturing continuum. We present a high-quality chromosome-level reference genome for U. stansburiana and pair it with RNA-seq gene expression data to demonstrate, for the first time, the molecular basis for pace-of-life differences between locations with higher and lower climate seasonality and sexual size dimorphism (SSD). Our assembly is 2.1 Gbp, has scaffold N50 of 320 Mbp, includes 104 scaffolds, and has an L50 of 3. The assembly comprises six macrochromosomes and 11 microchromosomes. We annotated 20,350 genes for the assembly and found a repeat element composition of 49.23%, similar to work in other phrynosomatid lizards. RNA-seq data demonstrate differential expression in genes associated with pace-of-life divergence including those related to stress, sexual reproduction, and cell proliferation/carcinogenesis between distinctive environments. Our results provide the first differential gene expression evidence of environmentally mediated pace-of-life processes related to different degrees of SSD in U. stansburiana and demonstrate the utility of RNA-seq gene expression data in detecting POLS.

Keywords: Baja California; RNA-seq; Uta stansburiana; chromosome-level genome assembly; pace-of-life syndrome; seasonality.

Figure 1.

A) Map of full range of Uta stansburiana (IUCN Redlist) with collection locality of specimen from which the reference genome was sequenced (DLE 3124) and the study area in Baja California, MX is highlighted. B) Photo of the individual male Uta stansburiana nevadensis (DLE 3124) from whom the reference genome was generated (photo courtesy Dr. Pete Zani). C) Map of samples collected for RNA with percentage of average total annual precipitation occurring in the winter (December-February; Fick and Hijmans 2017). Samples represent 33 specimens collected across seven sites. Sites were divided into those north (3 populations, 9 samples) and south (4 populations, 24 samples) of the Vizcaíno desert. D) Differences in temperature seasonality (standard deviation of monthly temperatures × 100, BIO4; Fick and Hijmans 2017) between northern and southern sites.

Figure 2.

Riparian plot of genomic syntenic blocks in four phrynosomatid reference genomes (Phrynosoma platirhinos, Sceloporus undulatus, Urosaurus nigricaudus, and Uta stansburiana) and one dactyloid (Anolis carolinensis) reference genome. Chromosome-level scaffolds have been re-named to reflect the position of each scaffold when sorted by length and appended with the first letter or first two letters of the genus. Suspected or identified X chromosomes are noted.

Figure 3.

A) Heatmap of log2-transformed count data for genes with differential expression by region, controlling for season and sex. Samples are labeled by region, season, and sex. B) Principal components analysis of regular log-transformed count data. PC2 and PC3 are shown here to better illustrate the distinctions between groups; see Fig S4 for PC1 and PC2. Ellipses enclose the centroids of the northern and southern samples.

Figure 4.

Volcano plot of genes differentially expressed between northern and southern groups, controlling for seasonal differences. Positive log2 fold change values correspond to genes differentially over-expressed in the southern group, while negative log2 fold change values correspond to genes differentially under-expressed in the southern group. ADAM20 is not plotted here, but see Fig. S5.