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Anatomy and dietary specialization influence sensory behaviour among sympatric primates.

ABSTRACT: Senses form the interface between animals and environments, and provide a window into the ecology of past and present species. However, research on sensory behaviours by wild frugivores is sparse. Here, we examine fruit assessment by three sympatric primates (Alouatta palliata, Ateles geoffroyi and Cebus imitator) to test the hypothesis that dietary and sensory specialization shape foraging behaviours. Ateles and Cebus groups are comprised of dichromats and trichromats, while all Alouatta are trichomats. We use anatomical proxies to examine smell, taste and manual touch, and opsin genotyping to assess colour vision. We find that the frugivorous spider monkeys (Ateles geoffroyi) sniff fruits most often, omnivorous capuchins (Cebus imitator), the species with the highest manual dexterity, use manual touch most often, and that main olfactory bulb volume is a better predictor of sniffing behaviour than nasal turbinate surface area. We also identify an interaction between colour vision phenotype and use of other senses. Controlling for species, dichromats sniff and bite fruits more often than trichromats, and trichromats use manual touch to evaluate cryptic fruits more often than dichromats. Our findings reveal new relationships among dietary specialization, anatomical variation and foraging behaviour, and promote understanding of sensory system evolution.

SUBMITTER: Melin AD

PROVIDER: S-EPMC9382214 | biostudies-literature | 2022 Aug

REPOSITORIES: biostudies-literature

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Anatomy and dietary specialization influence sensory behaviour among sympatric primates.

Melin Amanda D AD Veilleux Carrie C CC Janiak Mareike C MC Hiramatsu Chihiro C Sánchez-Solano Karem G KG Lundeen Ingrid K IK Webb Shasta E SE Williamson Rachel E RE Mah Megan A MA Murillo-Chacon Evin E Schaffner Colleen M CM Hernández-Salazar Laura L Aureli Filippo F Kawamura Shoji S

Proceedings. Biological sciences 20220817 1981

Senses form the interface between animals and environments, and provide a window into the ecology of past and present species. However, research on sensory behaviours by wild frugivores is sparse. Here, we examine fruit assessment by three sympatric primates (Alouatta palliata, Ateles geoffroyi and Cebus imitator) to test the hypothesis that dietary and sensory specialization shape foraging behaviours. Ateles and Cebus groups are comprised of dichromats and tri ...[more]

PMID: 35975434

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Project description:Effectively characterizing primate diets is fundamental to understanding primate behavior, ecology and morphology. Examining temporal variation in a species' diet, as well as comparing the responses of different species to variation in resource availability, can enhance understanding of the evolution of morphology and socioecology. In this study, we use feeding data collected over five years to describe the diets of two sympatric Southeast Asian primate species of similar body size: white-bearded gibbons (Hylobates albibarbis) and red leaf monkeys (Presbytis rubicunda rubida), in Gunung Palung National Park, West Kalimantan, Indonesia. Long-term data sets are especially important for characterizing primate diets in Southeast Asia, where the forests exhibit supra-annual mast fruiting events. We found that gibbons were mainly frugivorous, with fruit and figs comprising 70% of their 145 independent feeding observations, whereas leaf monkeys ate a substantial amount of seeds (26%), fruits and figs (26.5%) and leaves (30%, n = 219 independent feeding observations). Leaf monkeys consumed a higher number of plant genera, and this was due mostly to the non-frugivorous portion of their diet. To investigate resource selection by these primates we utilized two different approaches: the Manly Selectivity Ratio, which did not take into account temporal variation of resource availability, and a model selection framework which did incorporate temporal variation. Both species selected figs (Ficus) more than predicted based on their availability under the Manly Selectivity Ratio. Model selection allowed us to determine how these primates alter the proportion of leaves, flowers, seeds, figs and fruit in their diets in response to variation in fruit availability. When fruits were scarce, both gibbons and leaf monkeys incorporated more leaves and figs into their diets, indicating that these two food classes are fallback foods for these primates. We discuss how different measures of resource selection can provide seemingly contradictory results, and emphasize the importance of long term studies that combine independent feeding observations with rigorous assessment of temporal variation in resource availability when modelling feeding selectivity.

Project description:Sympatric speciation can arise as a result of disruptive selection with assortative mating as a pleiotropic by-product. Studies on host choice, employing artificial neural networks as models for the host recognition system in exploiters, illustrate how disruptive selection on host choice coupled with assortative mating can arise as a consequence of selection for specialization. Our studies demonstrate that a generalist exploiter population can evolve into a guild of specialists with an 'ideal free' frequency distribution across hosts. The ideal free distribution arises from variability in host suitability and density-dependent exploiter fitness on different host species. Specialists are less subject to inter-phenotypic competition than generalists and to harmful mutations that are common in generalists exploiting multiple hosts. When host signals used as cues by exploiters coevolve with exploiter recognition systems, our studies show that evolutionary changes may be continuous and cyclic. Selection changes back and forth between specialization and generalization in the exploiters, and weak and strong mimicry in the hosts, where non-defended hosts use the host investing in defence as a model. Thus, host signals and exploiter responses are engaged in a red-queen mimicry process that is ultimately cyclic rather then directional. In one phase, evolving signals of exploitable hosts mimic those of hosts less suitable for exploitation (i.e. the model). Signals in the model hosts also evolve through selection to escape the mimic and its exploiters. Response saturation constraints in the model hosts lead to the mimic hosts finally perfecting its mimicry, after which specialization in the exploiter guild is lost. This loss of exploiter specialization provides an opportunity for the model hosts to escape their mimics. Therefore, this cycle then repeats. We suggest that a species can readily evolve sympatrically when disruptive selection for specialization on hosts is the first step. In a sexual reproduction setting, partial reproductive isolation may first evolve by mate choice being confined to individuals on the same host. Secondly, this disruptive selection will favour assortative mate choice on genotype, thereby leading to increased reproductive isolation.

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Anatomy and dietary specialization influence sensory behaviour among sympatric primates.

Publications

Anatomy and dietary specialization influence sensory behaviour among sympatric primates.

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