Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory

Abstract

Primates possess remarkably variable color vision, and the ecological and social factors shaping this variation remain heavily debated. Here, we test whether central tenants of the folivory hypothesis of routine trichromacy hold for the foraging ecology of howler monkeys. Howler monkeys (genus Alouatta) and paleotropical primates (Parvorder: Catarrhini) have independently acquired routine trichromacy through fixation of distinct mid- to long-wavelength-sensitive (M/LWS) opsin genes on the X-chromosome. The presence of routine trichromacy in howlers, while other diurnal neotropical monkeys (Platyrrhini) possess polymorphic trichromacy, is poorly understood. A selective force proposed to explain the evolution of routine trichromacy in catarrhines-reliance on young, red leaves-has received scant attention in howlers, a gap we fill in this study. We recorded diet, sequenced M/LWS opsin genes in four social groups of Alouatta palliata, and conducted colorimetric analysis of leaves consumed in Sector Santa Rosa, Costa Rica. For a majority of food species, including Ficus trees, an important resource year-round, young leaves were more chromatically conspicuous from mature leaves to trichromatic than to hypothetical dichromatic phenotypes. We found that 18% of opsin genes were MWS/LWS hybrids; when combined with previous research, the incidence of hybrid M/LWS opsins in this species is 13%. In visual models of food discrimination ability, the hybrid trichromatic phenotype performed slightly poorer than normal trichromacy, but substantially better than dichromacy. Our results provide support for the folivory hypothesis of routine trichromacy. Similar ecological pressures, that is, the search for young, reddish leaves, may have driven the independent evolution of routine trichromacy in primates on separate continents. We discuss our results in the context of balancing selection acting on New World monkey opsin genes and hypothesize that howlers experience stronger selection against dichromatic phenotypes than other sympatric species, which rely more heavily on cryptic foods.

Keywords: Alouatta; Ficus; color vision; molecular evolution; opsin; polymorphism; primate evolution; sensory ecology.

Figure 1

Study subject and representative dietary items. An adult male howler monkey (Alouatta palliata) forages on leaves in Sector Santa Rosa, Área de Conservación Guanacaste (a). Like other member of this genus, both male and female mantled howler monkeys possess routine trichromacy based on a short‐wavelength (bluish)‐sensitive opsin and distinct mid (greenish)‐ and long (reddish)‐wavelength‐sensitive photopigments. Reflectance spectra and corresponding photographs of dietary plants consumed by howler monkeys in Sector Santa Rosa, Costa Rica show color variation in accordance with phenophase (b,c). Some species, including Ficus bullenoi (b), have immature leaves that change color from reddish to greenish as they mature. Exostema mexicanum (c) exemplifies species whose immature leaves (smaller leaves at terminus of branch) are similar in chromaticity to mature leaves. Reflectance spectra (insets) quantify mean chroma of immature leaves (light gray data points, n = 5 leaves) and mature leaves (dark gray data points, n = 5 leaves) along the visible spectrum (400–700 nm). Photographs were taken in Sector Santa Rosa by AD Melin (a,b) and A. Guadamuz (c)

Figure 2

Exemplary chromatograms of direct PCR‐sequencing for partial exon 3 and exon 5 of M/LWS opsin genes from (a) a female howler monkey with one standard LWS and one standard MWS opsin genes on each X chromosome and (b) a female howler with one X chromosome carrying a standard LWS and a standard MWS opsin genes and the other X chromosome carrying a standard LWS opsin gene and an M‐L hybrid opsin gene. Amino acid site number is indicated in the top row. Amino acid abbreviations are given in the second row. The nucleotide reads are indicated in the third row. Letters and chromatograms for adenine, guanine, cytosine, and thymine are colored with green, black, blue, and red, respectively. The three spectral tuning amino acid site numbers, 180, 277, and 285 are highlighted in blue and enclosed in boxes. The L‐type and M‐type amino acids at the three sites are colored with red and green, respectively. Amino acid heterozygosity is apparent at the three sites by the double peaks. Note that double peaks are approximately the same height except at site 285 of the normal plus hybrid opsin gene (b)

Figure 3

Chromaticity and luminance plots of eight dietary species. Chromaticity values show the color distance for (a) the standard trichromat phenotype and (b) the anomalous color vision phenotype along the red‐green color dimension (x‐axis; L/(L + M)) and along the blue‐yellow dimension (y‐axis; S/(L + M)). Greater values along the x‐axis indicate redder coloration, and greater values along the y‐axis indicate bluer coloration. Luminance values (x‐axis; log(L + M)) are plotted against the blue‐yellow chromatic axis (y‐axis) for (c) the standard trichromat phenotype and (d) the anomalous color vision phenotype. Lighter gray data points plot young leaves (circles—upper surface, squares—lower surface), and darker gray triangles plot mature leaves. Upper mature leaves are marked by upward facing triangles, lower mature leaves are marked by downward facing triangles

Figure 4

JND analysis histogram for young leaves observed against mature leaves: (a,c) upper leaf surfaces; (b,d) lower leaf surfaces. Histogram shows JND analysis in dark gray for standard trichromats (a,b) (T_LM) or anomalous trichromats (c,d), and in moderate gray for Dichromat M (D_M) and white for Dichromat L (D_L). The young leaves of species with less than one JND value (represented by a dashed line in both figures) are not predicted to be discernable to observers. A difference of more than one JND value between phenotypes signifies a predicted perceptual advantage. Albizia adinocephala (Aade), Albizia saman (Samanea saman; Ssam), Astronium graveolens (Agra), Bursera simarouba (Bsim), Chomelia spinose (Cspi), Exostema Mexicana (Emex), and Ficus bullenoi (Fbul), Gliricidia sepium (Gsep) (Table 1)

Figure 5

Circular heat maps of young leaf availability for 41 tree species in Sector Santa Rosa ordered from most to least synchronous in annual young leaf flush. The colored tiles show loess‐smoothed estimates of young‐leaf availability for each species, based on an availability index calculated for each individual tree of that species that was scored in that particular month and year (Campos et al., 2014). The availability index is an estimate of the proportion of the tree's canopy that is covered by new leaves. Fig trees (Ficus species, blue enlarged typeface) are among the most asynchronous and are often flush in young leaves when other species are not

Figure 6

Circular histograms showing the number of monitored plant species that are in peak phenophase during each month for mature leaves (green) and young leaves (orange). The month of peak phenophase for each species is based on monthly phenological records collected over a 9‐year period. The peak in young leaf availability coincides with the dry‐to‐wet season transition in May, while the peak in mature leaf availability coincides with the peak of the wet season in September