Identifying the causal factors that led to the evolution of traits characteristic of living primates has been a central focus in biological anthropology for over a century (Wood Jones, 1912). Functional interpretations of the set of traits that unites living primates and differentiates them from other living mammals informed early adaptive scenarios for primate origins. While an integrated ‘arboreal theory’ of primate origins suggesting the forward-facing eyes, high visual acuity, fine tactile sense, and postcranial adaptations that differentiate living primates from most other mammals evolved to facilitate life in the trees dominated the literature for decades (Wood Jones, 1916; Le Gros Clark, 1934, 1959), comparative morphological and behavioral data suggest that an arboreal habitat is not sufficient to explain the evolution of all traits characteristic of crown primates (Cartmill, 1974, 1992; Essner, 2007; Orkin and Pontzer, 2011; Urbani and Youlatos, 2013). Additionally, fossil evidence from both crown primates and plesiadapiform stem primates suggests that the common ancestor of these clades was already arboreal (Kirk et al., 2008). The two primate-origins hypotheses most frequently cited in recent decades focus on more specific aspects of the earliest crown primates' ecology. Each argues that the demands associated with a particular diet and method of foraging within the fine terminal branches of trees created selective pressures favoring the evolution of crown primates' distinguishing traits, including forward-facing eyes with parallel optic axes and the resulting wide field of binocular vision and precise depth perception.

The angiosperm–primate coevolution hypothesis (APCH) suggests that distinctive extant primate traits evolved to facilitate foraging on fruits and flowers in the terminal branches of flowering trees (Sussman and Raven, 1978; Sussman, 1991, 1995). Angiosperms became the dominant trees in late Cretaceous forests and developed specialized coevolutionary relationships with the birds and mammals that dispersed their seeds throughout the Paleocene (Tiffney, 2004). Noting this period's correlation with the timing of stem primate diversification, Sussman and Raven (1978) proposed that traits observed in living primates evolved to enable them to navigate the fine-branch niche, which contained these new food resources, as well as to manipulate and ingest angiosperm products. While much of the recent support for the APCH derives stem primate fossil material (Bloch and Boyer, 2002, 2007; Silcox and López-Torres, 2017) and forward-facing eyes evolved later at the crown primate node (Cartmill, 1974; Ross, 1995, 2000; Bloch et al., 2007), the APCH is still invoked as a potential explanation for the evolution of this diagnostic crown primate trait (Rasmussen and Sussman, 2007; Rosenberger, 2013; Sussman et al., 2013). In this adaptive scenario, the evolution of more parallel optic axes and a wide binocular field in early crown primates represents a second phase of adaptation to facilitate “feeding on and manipulating items of very small size (e.g., fruits, flowers, and insects), at very close range, and under low light conditions” (Sussman, 1991: 219). This scenario assumes that binocular depth cues would be important for grasping small fruit targets at close range.

The nocturnal visual predation hypothesis (NVPH) suggests that predation on insects in the fine branches of the trees led to the origin of crown primates and evolution of their distinctive visual traits. Cartmill (1974, 1992) noted that visually directed predators such as felid carnivores and owls tend to have forward-facing eyes similar to those of living primates and proposed that visually guided predation shaped the evolution of early crown primate traits (Cartmill, 1974). Allman (1977) and Pettigrew (1978) noted that having more parallel optic axes would specifically benefit nocturnal predatory species as this eye orientation provides a way to prevent the retinal image of objects in front of the animal from blurring due to spherical aberration without sacrificing image brightness by mitigating spherical aberration through pupil constriction. Cartmill (1992) incorporated this perspective from theoretical optics and proposed that predatory behavior, specifically in a nocturnal habitat, was responsible for the evolution of crown primate traits including parallel optic axes and a wide binocular field. Support for the NVPH has been derived largely from comparative studies of the function and ecomorphology of eye and bony orbit orientation across mammals (Ravosa et al., 2000, 2007; Ravosa and Savakova, 2004; Heesy, 2005, 2008).

Both the APCH and NVPH were originally proposed as explanations for the evolution of at least a portion of the suite of adaptations that differentiates living primates from other living mammals, which includes traits associated with grasping, leaping, visual system modifications, and herbivory. Fossil material increasingly suggests that these adaptations evolved in mosaic fashion (Bloch and Boyer, 2002; Bloch et al., 2007; Cartmill, 2012; Silcox et al., 2014) and therefore explaining their evolution via a single ecological condition or selective pressure is unlikely (Soligo and Smaers, 2016). Among the adaptations that have remained associated with the crown primate node are features of the visual system, including forward-facing eyes with parallel optic axes.

For an animal with a given monocular visual field and interocular distance, more parallel positioning of the optic axes increases the field of binocular overlap, within which, objects are seen with both eyes simultaneously. This eye orientation offers several benefits (recently reviewed in Read, 2021), several of which would be of particular importance to nocturnal animals living in light-limited environments, such as the earliest primates. Light is up to twice as likely to be detected in the binocular field as in the monocular visual fields (Pirenne, 1943; Warrant, 2008), and improved light sensitivity would be a significant advantage for nocturnal animals. Forward-facing eyes with more parallel optic axes also increase the acuity of an animal's vision in the region in front of their snout by reducing spherical aberration of light passing through the lens from this region (Pettigrew, 1978). Again, this advantage would be beneficial for species living in light-limited environments that preclude the use of pupillary constriction to facultatively counter spherical aberration. Contrast discrimination, the ability to detect luminance discrepancies between objects or among regions within an object, is also improved within the binocular field (Pirenne, 1943; Campbell and Green, 1965). And lastly, depth cues available within this binocular field are more precise than the depth cues that are available within the monocular visual field (Poggio and Poggio, 1984; Howard and Rogers, 1995; Plooy et al., 1998; Cumming and DeAngelis, 2001).

Both the NVPH and APCH propose that a grasping and/or manipulative behavior drove the evolution of primates' forward-facing eyes and wide binocular field (Cartmill, 1974, 1992; Sussman, 1991). The human clinical literature shows that the ability to use binocular cues significantly improves performance in grasping tasks similar to those invoked by the APCH and NVPH (Servos and Goodale, 1994; Fielder and Moseley, 1996; Grafton, 2010; Read et al., 2013; Bloch et al., 2015). Under monocular conditions, human individuals execute less accurate manual grasps and move their hands toward objects more slowly using a larger grasp aperture, reflecting their uncertainty about the position of the object (Servos and Goodale, 1994; Grafton, 2010; Read et al., 2013; Bloch et al., 2015). Binocular visual cues decrease the time required for an individual to accurately recognize the shape and size of an object in three dimensions, improving the speed and efficiency of grasping (Fielder and Moseley, 1996). These findings suggest that either the APCH or NVPH may present a reasonable explanation for the evolution of more parallel optic axes in the earliest crown primates. However, these clinical studies evaluated the effect of the presence vs. total absence of binocular vision in humans. As haplorhines, humans also have a visual system that is highly derived in terms of acuity and neuroanatomy compared to the condition inferred for early crown primates (Barton, 1998, Ross, 2000, Preuss, 2007; Kirk, 2004, Martin and Ross, 2005; Kirk and Kay, 2004). Therefore, meaningfully evaluating whether the APCH and/or NVPH is a viable explanation for the evolution of primates' derived optic axis orientation relative to other euarchontans requires an understanding of how binocular cues affect insect and fruitgrasping performance in species morphologically and ecologically similar to early crown primates.

This study experimentally tests how availability of binocular visual cues influences the ability of two species of cheirogaleids (Cheirogaleus medius and Microcebus murinus) to grasp fruit and insect targets. While their origin and diversification are far removed from the crown primate node (Andrews et al., 2016), cheirogaleids are often considered the best extant primate analogs of the earliest crown primates (Martin, 1972a) due to their mix of generalized arboreal quadrupedalism and leaping locomotion (Boyer et al., 2013a; Marigó et al., 2016), small body size (Gingerich, 1986; Gebo, 2004; Ni et al., 2004; but see Soligo and Martin, 2006), nocturnal visual ecology (Melin et al., 2016), and omnivorous diet (Hladik et al., 1980; Atsalis, 1999). Determining whether increased availability of binocular depth cues provides a performance advantage in the behaviors invoked by the APCH and NVPH in these species allows for an evaluation of whether the adaptive scenarios proposed by the APCH and NVPH provide viable mechanisms for the evolution of crown primates' forward-facing eyes and resultant wide binocular field. Collecting these data in two cheirogaleid species that differ to varying degrees in their relative hand size Lemelin and Jungers, 2007, visual adaptations (Veilleux et al., 2013; Melin et al., 2016), and degree of insectivory (Radespiel et al., 2006; Lahann, 2007) allows a more nuanced interpretation of the experimental results and consideration of how specific attributes of each species may impact their performance in the standardized grasping tasks.