Transcriptomic regulation of seasonal coat color change in hares

Abstract

Color molts from summer brown to winter white coats have evolved in several species to maintain camouflage year‐round in environments with seasonal snow. Despite the eco‐evolutionary relevance of this key phenological adaptation, its molecular regulation has only recently begun to be addressed. Here, we analyze skin transcription changes during the autumn molt of the mountain hare (Lepus timidus) and integrate the results with an established model of gene regulation across the spring molt of the closely related snowshoe hare (L. americanus). We quantified differences in gene expression among three stages of molt progression—“brown” (early molt), “intermediate,” and “white” (late molt). We found 632 differentially expressed genes, with a major pulse of expression early in the molt, followed by a milder one in late molt. The functional makeup of differentially expressed genes anchored the sampled molt stages to the developmental timeline of the hair growth cycle, associating anagen to early molt and the transition to catagen to late molt. The progression of color change was characterized by differential expression of genes involved in pigmentation, circadian, and behavioral regulation. We found significant overlap between differentially expressed genes across the seasonal molts of mountain and snowshoe hares, particularly at molt onset, suggesting conservatism of gene regulation across species and seasons. However, some discrepancies suggest seasonal differences in melanocyte differentiation and the integration of nutritional cues. Our established regulatory model of seasonal coat color molt provides an important mechanistic context to study the functional architecture and evolution of this crucial seasonal adaptation.

The Legacy of Recurrent Introgression during the Radiation of Hares

“…The functions of these introgressed genes overlap with common physiological adaptations of northern latitude animals to seasonal conditions, such as higher metabolic rates, regulation of body temperature and nonshivering thermogenesis ( Hart et al 1965 ; Feist and Rosenmann 1975 ; Rogowitz 1990 ; Pyörnilä et al 2008 ; Sheriff et al 2009 ), seasonal camouflage ( Grange 1932 ; Hewson 1958 ; Hansen and Bear 1963 ; Mills et al 2018 ; Zimova et al 2018 ), and visual acuity in response to dim winter light in northern latitudes ( Stokkan et al 2013 ). Furthermore, the functions of two of these genes, pigmentation and circadian rhythms, are linked to pathways activated during seasonal coat color changing molts ( Ferreira et al 2017 , 2020 ). The functional relevance of these candidates to local adaptation must await further testing.…”

Hybridization with mountain hares increases the functional allelic repertoire in brown hares

“…Adaptive advantage of the local alleles should manifest as overrepresentation of mountain hare alleles in brown hares that exceeds the levels expected from random genetic drift. In fact, previous studies have shown that hybridization with closely related species has provided both snowshoe hares ( Lepus americanus Erxleben) 11 – 15 and mountain hares 16 – 18 with beneficial alleles related to winter pelage color. Due to the shorter snow-covered season, camouflage mismatch with white winter pelage on bare ground has been shown to carry fitness costs 19 , which cannot be compensated through adaptive behavioral plasticity 20 .…”

Assembly-free rapid differential gene expression analysis in non-model organisms using DNA-protein alignment

“…On the other hand, driven by declining costs, RNA-seq is becoming increasingly accessible to labs with modest resources; and as a result, it is being employed on an everexpanding catalog of non-model organisms, pervading the fields of agriculture, aquaculture, ecology, and environment. A very short list of recent studies include: environmental stress response in sea-trout [3], coral [4], ryegrass [5], pigeonpea [6], tiger barb [7]; immune response to parasites and pathogens in guppy [8], eel [9], silkworm [10], peanut [11], sunflower [12]; mechanisms of phenotypic divergence in hares [13], bats [14], grass carps [15]; effect of diet in the growth and development in shrimp [16], yellow perch [17], mandarin fish [18], grenadier anchovy [19], catfish [20], tilapia [21], bass [22]. It is only likely that RNA-seq will continue to rapidly proliferate while high-quality reference databases grow at a slow pace.…”