Gillian L. Moritz

Why Aye-Ayes See Blue

The capacity for cone‐mediated color vision varies among nocturnal primates. Some species are colorblind, having lost the functionality of their short‐wavelength‐sensitive‐1 (SWS1) opsin pigment gene. In other species, such as the aye‐aye (Daubentonia madagascariensis), the SWS1 gene remains intact. Recent studies focused on aye‐ayes indicate that this gene has been maintained by natural selection and that the pigment has a peak sensitivity (λmax) of 406 nm, which is ∼20 nm closer to the ultraviolet region of the spectrum than in most primates. The functional significance behind the retention and unusual λmax of this opsin pigment is unknown, and it is perplexing given that all mammals are presumed to be colorblind in the dark. Here we comment on this puzzle and discuss recent findings on the color vision intensity thresholds of terrestrial vertebrates with comparable optics to aye‐ayes. We draw attention to the twilight activities of aye‐ayes and report that twilight is enriched in short‐wavelength (bluish) light. We also show that the intensity of twilight and full moonlight is probably sufficient to support cone‐mediated color vision. We speculate that the intact SWS1 opsin pigment gene of aye‐ayes is a crepuscular adaptation and we report on the blueness of potential visual targets, such as scent marks and the brilliant blue arils of Ravenala madagascariensis.

Inferred L/M cone opsin polymorphism of ancestral tarsiers sheds dim light on the origin of anthropoid primates

Tarsiers are small nocturnal primates with a long history of fuelling debate on the origin and evolution of anthropoid primates. Recently, the discovery of M and L opsin genes in two sister species, Tarsius bancanus (Bornean tarsier) and Tarsius syrichta (Philippine tarsier), respectively, was interpreted as evidence of an ancestral long-to-middle (L/M) opsin polymorphism, which, in turn, suggested a diurnal or cathemeral (arrhythmic) activity pattern. This view is compatible with the hypothesis that stem tarsiers were diurnal; however, a reversion to nocturnality during the Middle Eocene, as evidenced by hyper-enlarged orbits, predates the divergence of T. bancanus and T. syrichta in the Late Miocene. Taken together, these findings suggest that some nocturnal tarsiers possessed high-acuity trichromatic vision, a concept that challenges prevailing views on the adaptive origins of the anthropoid visual system. It is, therefore, important to explore the plausibility and antiquity of trichromatic vision in the genus Tarsius. Here, we show that Sulawesi tarsiers (Tarsius tarsier), a phylogenetic out-group of Philippine and Bornean tarsiers, have an L opsin gene that is more similar to the L opsin gene of T. syrichta than to the M opsin gene of T. bancanus in non-synonymous nucleotide sequence. This result suggests that an L/M opsin polymorphism is the ancestral character state of crown tarsiers and raises the possibility that many hallmarks of the anthropoid visual system evolved under dim (mesopic) light conditions. This interpretation challenges the persistent nocturnal–diurnal dichotomy that has long informed debate on the origin of anthropoid primates.

Primate communication in the pure ultrasound.

Few mammals—cetaceans, domestic cats and select bats and rodents—can send and receive vocal signals contained within the ultrasonic domain, or pure ultrasound (greater than 20 kHz). Here, we use the auditory brainstem response (ABR) method to demonstrate that a species of nocturnal primate, the Philippine tarsier (Tarsius syrichta), has a high-frequency limit of auditory sensitivity of ca 91 kHz. We also recorded a vocalization with a dominant frequency of 70 kHz. Such values are among the highest recorded for any terrestrial mammal, and a relatively extreme example of ultrasonic communication. For Philippine tarsiers, ultrasonic vocalizations might represent a private channel of communication that subverts detection by predators, prey and competitors, enhances energetic efficiency, or improves detection against low-frequency background noise.

A novel method for comparative analysis of retinal specialization traits from topographic maps

Vertebrates possess different types of retinal specializations that vary in number, size, shape, and position in the retina. This diversity in retinal configuration has been revealed through topographic maps, which show variations in neuron density across the retina. Although topographic maps of about 300 vertebrates are available, there is no method for characterizing retinal traits quantitatively. Our goal is to present a novel method to standardize information on the position of the retinal specializations and changes in retinal ganglion cell (RGC) density across the retina from published topographic maps. We measured the position of the retinal specialization using two Cartesian coordinates and the gradient in cell density by sampling ganglion cell density values along four axes (nasal, temporal, ventral, and dorsal). Using this information, along with the peak and lowest RGC densities, we conducted discriminant function analyses (DFAs) to establish if this method is sensitive to distinguish three common types of retinal specializations (fovea, area, and visual streak). The discrimination ability of the model was higher when considering terrestrial (78%-80% correct classification) and aquatic (77%-86% correct classification) species separately than together. Our method can be used in the future to test specific hypotheses on the differences in retinal morphology between retinal specializations and the association between retinal morphology and behavioral and ecological traits using comparative methods controlling for phylogenetic effects.

Technical Note: Calcium and carbon stable isotope ratios as paleodietary indicators.

Calcium stable isotope ratios are hypothesized to vary as a function of trophic level. This premise raises the possibility of using calcium stable isotope ratios to study the dietary behaviors of fossil taxa and to test competing hypotheses on the adaptive origins of euprimates. To explore this concept, we measured the stable isotope composition of contemporary mammals in northern Borneo and northwestern Costa Rica, two communities with functional or phylogenetic relevance to primate origins. We found that bone collagen δ(13) C and δ(15) N values could differentiate trophic levels in each assemblage, a result that justifies the use of these systems to test the predicted inverse relationship between bioapatite δ(13) C and δ(44) Ca values. As expected, taxonomic carnivores (felids) showed a combination of high δ(13) C and low δ(44) Ca values; however, the δ(44) Ca values of other faunivores were indistinguishable from those of primary consumers. We suggest that the trophic insensitivity of most bioapatite δ(44) Ca values is attributable to the negligible calcium content of arthropod prey. Although the present results are inconclusive, the tandem analysis of δ(44) Ca and δ(13) C values in fossils continues to hold promise for informing paleodietary studies and we highlight this potential by drawing attention to the stable isotope composition of the Early Eocene primate Cantius.

Conservation Genetics of the Philippine Tarsier: Cryptic Genetic Variation Restructures Conservation Priorities for an Island Archipelago Primate

Establishment of conservation priorities for primates is a particular concern in the island archipelagos of Southeast Asia, where rates of habitat destruction are among the highest in the world. Conservation programs require knowledge of taxonomic diversity to ensure success. The Philippine tarsier is a flagship species that promotes environmental awareness and a thriving ecotourism economy in the Philippines. However, assessment of its conservation status has been impeded by taxonomic uncertainty, a paucity of field studies, and a lack of vouchered specimens and genetic samples available for study in biodiversity repositories. Consequently, conservation priorities are unclear. In this study we use mitochondrial and nuclear DNA to empirically infer geographic partitioning of genetic variation and to identify evolutionarily distinct lineages for conservation action. The distribution of Philippine tarsier genetic diversity is neither congruent with expectations based on biogeographical patterns documented in other Philippine vertebrates, nor does it agree with the most recent Philippine tarsier taxonomic arrangement. We identify three principal evolutionary lineages that do not correspond to the currently recognized subspecies, highlight the discovery of a novel cryptic and range-restricted subcenter of genetic variation in an unanticipated part of the archipelago, and identify additional geographically structured genetic variation that should be the focus of future studies and conservation action. Conservation of this flagship species necessitates establishment of protected areas and targeted conservation programs within the range of each genetically distinct variant of the Philippine tarsier.

Thermal Imaging of Aye-Ayes (Daubentonia madagascariensis) Reveals a Dynamic Vascular Supply During Haptic Sensation

Infrared thermography (IRT) is used to visualize and estimate variation in surface temperatures. Applications of IRT to animal research include studies of thermofunctional anatomy, ecology, and social behavior. IRT is especially amenable to investigations of the somatosensory system because touch receptors are highly vascularized, dynamic, and located near the surface of the skin. The hands of aye-ayes (Daubentonia madagascariensis) are thus an inviting subject for IRT because of the prominent middle digit that functions as a specialized haptic sense structure during percussive and probative foraging. It is a vital sensory tool that is expected to feature a high density of dermal mechanoreceptors that radiate heat and impose thermal costs under cool temperatures. Here we explore this premise by acquiring IRT images of 8 aye-ayes engaged in a variety of passive and probative behaviors. We found that the middle digit was typically 2.3°C cooler than other digits when the metacarpophalangeal (MP) joint was extended, and that it warmed an average of 2.0°C when the MP joint was flexed during active touching behavior. These changes in digital surface temperature, which were sometimes as much 6.0°C, stand in sharp contrast with the profoundly invariant temperatures of the other digits. Although the physiological mechanisms behind these temperature changes are unknown, they appear to reveal a uniquely dynamic vascular supply.

Niche convergence suggests functionality of the nocturnal fovea

The fovea is a declivity of the retinal surface associated with maximum visual acuity. Foveae are widespread across vertebrates, but among mammals they are restricted to haplorhine primates (tarsiers, monkeys, apes, and humans), which are primarily diurnal. Thus primates have long contributed to the view that foveae are functional adaptations to diurnality. The foveae of tarsiers, which are nocturnal, are widely interpreted as vestigial traits and therefore evidence of a diurnal ancestry. This enduring premise is central to adaptive hypotheses on the origins of anthropoid primates; however, the question of whether tarsier foveae are functionless anachronisms or nocturnal adaptations remains open. To explore this question, we compared the diets of tarsiers (Tarsius) and scops owls (Otus), taxa united by numerous anatomical homoplasies, including foveate vision. A functional interpretation of these homoplasies predicts dietary convergence. We tested this prediction by analyzing stable isotope ratios that integrate dietary information. In Borneo and the Philippines, the stable carbon isotope compositions of Tarsius and Otus were indistinguishable, whereas the stable nitrogen isotope composition of Otus was marginally higher than that of Tarsius. Our results indicate that species in both genera consumed mainly ground-dwelling prey. Taken together, our findings support a functional interpretation of the many homoplasies shared by tarsiers and scops owls, including a retinal fovea. We suggest that the fovea might function similarly in tarsiers and scops owls by calibrating the auditory localization pathway. The integration of auditory localization and visual fixation during prey detection and acquisition might be critical at low light levels.

Structure and Function of Regional Specializations in the Vertebrate Retina

Visual sensory demands vary substantially across vertebrates. Different visual sensory components have evolved to meet these sensory demands and enhance visual behavioral performance. One of these components is the retinal specialization, which is a portion of the retina with generally high ganglion cell densities, which increase spatial resolving power. Retinal specializations are relevant from a functional perspective because animals can align these “acute zones” with objects of interest within a localized region of their visual space, consequently affecting different behavioral dimensions. In this chapter, we reviewed the different types of retinal specializations found in vertebrates (retinal area , fovea, visual streak, radial anisotropy, area gigantocellularis) by discussing the different hypotheses proposed over decades to explain their function. Empirical tests on the functional properties of these different retinal specializations have been limited, which constrains our ability to understand the functional evolution of the vertebrate eye. We derive specific predictions from each of the hypotheses put forward to identify their degree of overlap. Finally, we provide some future directions as to how to test these functional hypotheses by integrating physiological and behavioral approaches. Testing these functional hypotheses will enhance our understanding of the relationship between the eye and the physical environment, and ultimately the visual ecology of vertebrates.

Baboons, Water, and the Ecology of Oxygen Stable Isotopes in an Arid Hybrid Zone

Baboons regularly drink surface waters derived from atmospheric precipitation, or meteoric water. As a result, the oxygen isotope (δ18O) composition of their tissues is expected to reflect that of local meteoric waters. Animal proxies of the oxygen isotope composition of meteoric water have practical applications as paleoenvironmental recorders because they can be used to infer aridity and temperature in historic and fossil systems. To explore this premise, we measured the δ18O values of hair from two baboon species, Papio anubis and Papio hamadryas, inhabiting Awash National Park, Ethiopia. The hybridizing taxa differ in their ranging behavior and physiological response to heat. Papio hamadryas ranges more widely in the arid thornbush and is inferred to ingest a greater proportion of leaf water that is enriched in 18O as a result of evaporative fractionation. It is also better able to conserve body water, which reduces its dependence on meteoric waters depleted in 18O. Taken together, these factors would predict relatively higher δ18O values in the hair (δ18Ohair) of P. hamadryas. We found that the δ18Ohair values of P. hamadryas were higher than those of P. anubis, yet the magnitude of the difference was marginal. We attribute this result to a common source of drinking water, the Awash River, and the longer drinking bouts of P. hamadryas. Our findings suggest that differences in δ18O values among populations of Papio (modern or ancient) reflect different sources of drinking water (which might have ecological significance) and, further, that Papio has practical value as a paleoenvironmental recorder.