Biodiversity Journal, 2016, 7 (1): 117–198 MONOGRAPH On the origin of allopatric primate species Marc G.M. van Roosmalen* & Tomas van Roosmalen ¹MVRS - Marc van Roosmalen Stichting, Leiden, The Netherlands *Corresponding author, e-mail: [email protected] ABSTRACT Here we present a theory on the origin of allopatric primate species that follows - at least in Neotropical primates - the irreversible trend to albinotic skin and coat color, called “meta- chromic bleaching”. It explains why primates constitute such an exceptionally diverse, species-rich, and colorful Order in the Class Mammalia. The theory is in tune with the principle of evolutionary change in tegumentary colors called “metachromism”, a hypothesis propounded by the late Philip Hershkovitz. Metachromism holds the evolutionary change in hair, skin, and eye melanins following an orderly and irreversible sequence that ends in loss of pigment becoming albinotic, cream to silvery or white. In about all extant sociable Neo- tropical monkeys we identified an irreversible trend according to which metachromic varieties depart from the saturated eumelanin (agouti, black or blackish brown) archetypic form and then speciate into allopatric taxa following the trend to albinotic skin and coat color. Speci- ation goes either along the eumelanin pathway (from gray to silvery to cream to white), or the pheomelanin pathway (from red to orange to yellow to white), or a combination of the two. The theory represents a new and original evolutionary concept that seems to act indef- initely in a non-adaptive way in the population dynamics of male-hierarchic societies of all sociable primates that defend a common territory. We have successfully tested the theory in all 19 extant Neotropical monkey genera. Our theory suggests the trend to allopatry among metachromic varieties in a social group or population to be the principal behavioral factor that empowers metachromic processes in sociable Neotropical monkeys. It may well represent the principal mechanism behind speciation, radiation, niche separation, and phylogeography in all sociable primates that hold male-defended territories. We urge field biologists who study primate distributions, demography and phylogeography in the Old World to take our theory to the test in the equally colorful Catarrhini. KEY WORDS Neotropical primates; phylogeography; metachromic bleaching; speciation; radiation. Received 20.12.2015; accepted 09.02.2016; printed 30.03.2016 INTRODUCTION organized social structure and male territoriality? If not sexual selection, what could be the principal We could ask ourselves (Darwin, 1859): “Why factor(s) in primate social behavior to be held primates constitute by far the most diverse, species- rich and colorful Order in the Class Mammalia? responsible for metachromic processes, speciation, Do primate diversity, metachromism and meta- radiation, niche separation, and phylogeography?” chromic processes relate directly to sexual selection? Inspired by Alfred Russel Wallace whose concept Or, rather to its generally complex, hierarchically of the “Origin of Species” was laid down in a paper 118 MARC G.M. VAN ROOSMALEN & TOMAS VAN ROOSMALEN he sent for review to Charles Darwin, here we introduce a new and original theory about species evolution taking place in particular in sociable territorial primates. Our theory “On the tendency of metachromic varieties in sociable primates to depart indefinitely from the agouti archetype and evolve in advanced eumelanin, pheomelanin to albinotic bleached allopatric taxa” is equally rooted in life-long fieldwork on socio-ecology of all Neo- tropical monkey genera, both in captivity and in the wild. It closely follows the principle of evolutionary change in tegumentary colors called “meta- chromism”, a hypothesis propounded by Philip Figure 1. Bleaching from saturated eumelanin and saturated Hershkovitz (1968; 1977). Metachromism holds the pheomelanin fields to white or colorless. Gradual reduction evolutionary change in hair, skin, and eye melanins in the amount of pigment deposited in the growing hair re- following an orderly and irreversible sequence that sults in apparent change from blackish through brown, drab gray to white or colorless in the eumelanin pathway, and ends in loss of pigment through which a taxon of a from reddish through orange, yellow, cream to white in the given genus or phylogenetic clade eventually be- pheomelanin pathway. Switching from the eumelanin to the comes albinotic, cream to white. Individual hair pheomelanin pathway occurs in saturation but not in blea- color or the entire coat changes from agouti (char- ching (modified from Hershkovitz, 1977). acterized by alternating blackish-brown and reddish bands on the terminal half of the hair) to uniformly blackish-brown, and thereafter to gray, and even- neotonic, taking place locally (e.g., naked muzzle, tually to white or colorless, called the eumelanin bald head, euchromic blaze/forehead or part of the pathway; or, it changes from agouti to uniformly coat, depilation of skin) or all over the body. Social reddish to orange to yellow to cream, and even- structure in most primate societies, in particular tually white, called the pheomelanin pathway. The those of the more advanced monkeys and apes, is process itself is called saturation, which means the hierarchically organized, whereas male over female change from the primitive agouti pattern of the hair, dominance is the rule, with very few exceptions or part of the pelage, or the entire coat, to a satur- (e.g., spider monkeys in the Neotropics and pygmy ated eumelanin (blackish) or saturated pheomelanin chimpanzees in Central Africa adopted a matri- (reddish) coloration. The dilution, or gradual reduc- archal social system, in which males patrol and tion in the amount of pigment deposited in the defend a common territory, and females are allowed growing hair, and disappearance of pigmentary to transfer to neighboring social groups). Social colors is called bleaching (Fig. 1). In the color of selection is the recognition of and preference for the the skin and iris of the eye, it follows the eumelanin parental (or foster parental) phenotype in societal pathway (brown to drab, to gray, or blue), and then grouping and mating. Social selection for color or it is termed depigmentation. Metachromism applies color pattern through assortative mating tends to to all mammalian species. It is thought to also occur stabilize within a chromatic range recognized and in bird feathers. accepted by free-ranging but chromotypically Our theory suggests that among social groups imprinted members of the social group. Slightly or populations of advanced intelligent, socially depilated or somewhat eumelanin or pheomelanin organized, male-territorial mammals, in particular bleached individuals deviant from the socially primates, phenotypical varieties (mutants) that selected skin or hair color pattern, in particular show slightly bleached eumelanin or pheomelanin when it is detected in adolescent to subadult males, colored skin or coat characteristics do arise indef- may be discriminated against by high-ranking initely. Their melanocytes (skin cells that produce (alpha)-males. For that reason alone they can be the black pigment melanin) are smaller, and for that pushed into the periphery of the group. Depending or any other reason produce less melanin. In gen- on the primate taxon or genus, such individual eral, the tendency of these metachromic varieties is young males may also be expelled from the parental On the origin of allopatric primate species 119 group, and then become social ‘outcasts’. Peri- successively isolated breeding colony is, or the pheral or outcast males do suffer on a daily base farther it has moved from the center of that taxon’s from less and shorter access to the group’s prefer- dispersion, the nearer it will come to the end of its ential, comparatively more nutritious food sources. metachromic evolution. And, the narrower will be They may join one another for reasons of social its range of chromic fitness (e.g., prey and predator comfort and during ranging or foraging they tend camouflage). This degenerative process, though, to hang out together at the periphery of the group. may be counterbalanced if under strong natural Eventually, they may decide to leave the pack as selection newly diverged forms, that evolve in a, for all-male parties and roam around in much larger the original species marginal or new habitat, niche areas than just the home range or territory of the or landscape, at the same time selectively become parental group. They then may attract young fe- better fitted, more cooperative, more inventive, or males from neighboring social groups. Together, smarter in the adaptation process. This may happen they may seek some hitherto overlooked, ‘empty’ every time founder-colonies successfully travel or little-used living space in an attempt to settle across existing geographical barriers, such as rivers, down and start their own family or social group. In watersheds, mountain ranges, or open areas with case the taxon or genus it belongs to shows ter- arid scrub vegetation. Completion of the processes ritorial behavior - which is the case in almost all of metachromic bleaching, depigmentation, or de- Neotropical monkeys - these emigrants will be sub- pilation, whether taking place single or combined, sequently pushed out from neighboring territories eventually will result in extinction of the race or as well. Consequently, they will die from starvation,