Spiny mice modulate eumelanin to pheomelanin ratio to achieve cryptic coloration in "evolution canyon," Israel

Abstract

Background: Coat coloration in mammals is an explicit adaptation through natural selection. Camouflaging with the environment is the foremost evolutionary drive in explaining overall coloration. Decades of enquiries on this topic have been limited to repetitive coat color measurements to correlate the morphs with background/habitat blending. This led to an overwhelming endorsement of concealing coloration as a local phenotypic adaptation in animals, primarily rodents to evade predators. However, most such studies overlooked how rodents actually achieve such cryptic coloration. Cryptic coloration could be attained only through optimization between the yellow- to brown-colored "pheomelanin" and gray to black-colored "eumelanin" in the hairs. However, no study has explored this conjecture yet. "Evolution Canyon" (EC) in Israel is a natural microscale laboratory where the relationship between organism and environment can be explored. EC is comprised of an "African" slope (AS), which exhibits a yellow-brownish background habitat, and a "European" slope (ES), exhibiting a dark grayish habitat; both slopes harbor spiny mice (Acomys cahirinus). Here, we examine how hair melanin content of spiny mice living in the opposing slopes of EC evolves toward blending with their respective background habitat.

Methodology/principal findings: We measured hair-melanin (both eumelanin and pheomelanin) contents of 30 spiny mice from the EC using high-performance liquid chromatography (HPLC) that detects specific degradation products of eumelanin and pheomelanin. The melanin pattern of A. cahirinus approximates the background color of the slope on which they dwell. Pheomelanin is slightly (insignificantly) higher in individuals found on the AS to match the brownish background, whereas individuals of the ES had significantly greater eumelanin content to mimic the dark grayish background. This is further substantiated by a significantly higher eumelanin and pheomelanin ratio on the ES than on the AS.

Conclusion/significance: It appears that rodents adaptively modulate eumelanin and pheomelanin contents to achieve cryptic coloration in contrasting habitats even at a microscale.

Figure 1. “Evolution Canyon” (EC), Nahal Oren, Israel.

(A) aerial view and (B) cross-section showing the opposing slopes. Note the two habitat types; dry, open habitat (with light colored background) on the “African” slope and humid, closed habitat (with dark-colored background) in the “European” slope.

Figure 2. Habitat divergence in “Evolution Canyon”.

(A) photo showing part of the “African” slope (AS)/south-facing slope (SFS) of EC, characterized by light terra rossa soil with a stretch of grass cover that generates a yellow-brownish background. (B) Photo of part of the “European” slope (ES)/north-facing slope (NFS), characterized by dark terra rossa soil and shady, humus-laden dark background.

Figure 3. Differences in color morphs of spiny mice.

(Lateral view: (A,B) and dorsal view: (C,D) inhabiting “African” slope (A,C) and “European” slope (B,D) of Evolution Canyon I, Israel.

Figure 4. Contents of eumelanin and pheomelanin in hairs of spiny mice (Acomys cahirinus) from “Evolution Canyon” I, Israel.

(A) in the opposite slopes, (B) across stations. Means with the same letter are not significantly different according to Waller-Duncan k-ratio t-test.

Figure 5. Eumelanin/Pheomelanin ratio of A. cahirinus from “Evolution Canyon” I, Israel.

(A) in the opposite slopes, (B) across stations. Means with the same letter are not significantly different according to Waller-Duncan k-ratio t-test.