The potential interplay between the glandular microbiome and scent marking behavior in owl monkeys (Aotus nancymaae).

In mammals, scent marking behavior is a pervasive form of chemical communication that regulates social interactions within and between groups. Glandular microbiota consist of bacterial communities capable of producing chemical cues used in olfactory communication. Despite countless studies on scent marking in primates, few have examined the microbiota associated with glandular secretions. Nancy Ma's owl monkeys (Aotus nancymaae) are nocturnal, socially monogamous primates that frequently scent mark using their subcaudal glands. Previous analyses revealed that unique chemical signatures of Aotus may convey information about sex and age. We used positive reinforcement to sample the subcaudal glands of 23 captive owl monkeys to describe their glandular microbiomes and examine how patterns in these bacterial communities vary with age, sex, rearing environment and/or social group (pair identity). We coupled these analyses with behavioral observations to examine patterns in their scent marking behavior. We isolated 31 bacterial species from Phyla Firmicutes, Proteobacteria, and Actinobacteria, consistent with the dermal and glandular microbiomes of other primates. Several bacterial taxa we identified produce volatile organic compounds, which may contribute to olfactory communication. These bacterial communities are best predicted by an interaction between sex, rearing environment and pair identity rather than any of these variables alone. Within mated pairs of A. nancymaae, males and females scent mark their nest boxes at similar frequencies. In some pairs, rates of scent marking by males and females fluctuated over time in a similar manner. Pairs that had been together longer tended to exhibit the greatest similarities in their rates of scent marking. Together, these findings suggest that scent marking behavior and close social interactions with pair mates in Aotus may influence bacterial transmission and their glandular microbiomes. Chemical communication, including coordinated scent marking, may play a role in strengthening pair bonds, signaling pair status and/or in mate guarding in this socially monogamous primate.

Ancient and Recent Duplications Support Functional Diversity of Daphnia Opsins.

Daphnia pulex has the largest known family of opsins, genes critical for photoreception and vision in animals. This diversity may be functionally redundant, arising from recent processes, or ancient duplications may have been preserved due to distinct functions and independent contributions to fitness. We analyzed opsins in D. pulex and its distant congener Daphnia magna. We identified 48 opsins in the D. pulex genome and 32 in D. magna. We inferred the complement of opsins in the last common ancestor of all Daphnia and evaluated the history of opsin duplication and loss. We further analyzed sequence variation to assess possible functional diversification among Daphnia opsins. Much of the opsin expansion occurred before the D. pulex-D. magna split more than 145 Mya, and both Daphnia lineages preserved most ancient opsins. More recent expansion occurred in pteropsins and long-wavelength visual opsins in both species, particularly D. pulex. Recent duplications were not random: the same ancestral genes duplicated independently in each modern species. Most ancient and some recent duplications involved differentiation at residues known to influence spectral tuning of visual opsins. Arthropsins show evidence of gene conversion between tandemly arrayed paralogs in functionally important domains. Intron-exon gene structure was generally conserved within clades inferred from sequences, although pteropsins showed substantial intron size variation. Overall, our analyses support the hypotheses that diverse opsins are maintained due to diverse functional roles in photoreception and vision, that functional diversification is both ancient and recent, and that multiple evolutionary processes have influenced different types of opsins.

Ecological constraints on sensory systems: compound eye size in Daphnia is reduced by resource limitation.

Eye size is an indicator of visual capability, and macroevolutionary patterns reveal that taxa inhabiting dim environments have larger eyes than taxa from bright environments. This suggests that the light environment is a key driver of variation in eye size. Yet other factors not directly linked with visual tasks (i.e., non-sensory factors) may influence eye size. We sought to jointly investigate the roles of sensory (light) and non-sensory factors (food) in determining eye size and ask whether non-sensory factors could constrain visual capabilities. We tested environmental influences on eye size in four species of the freshwater crustacean Daphnia, crossing bright and dim light levels with high and low resource levels. We measured absolute eye size and eye size relative to body size in early and late adulthood. In general, Daphnia reared on low resources had smaller eyes, both absolutely and relatively. In contrast to the dominant macroevolutionary pattern, phenotypic plasticity in response to light was rarely significant. These patterns of phenotypic plasticity were true for overall diameter of the eye and the diameter of individual facets. We conclude that non-sensory environmental factors can influence sensory systems, and in particular, that resource availability may be an important constraint on visual capability.

Population genomics of resource exploitation: insights from gene expression profiles of two Daphnia ecotypes fed alternate resources.

Consumer-resource interactions are a central issue in evolutionary and community ecology because they play important roles in selection and population regulation. Most consumers encounter resource variation at multiple scales, and respond through phenotypic plasticity in the short term or evolutionary divergence in the long term. The key traits for these responses may influence resource acquisition, assimilation, and/or allocation. To identify relevant candidate genes, we experimentally assayed genome-wide gene expression in pond and lake Daphnia ecotypes exposed to alternate resource environments. One was a simple, high-quality laboratory diet, Ankistrodesmus falcatus. The other was the complex natural seston from a large lake. In temporary ponds, Daphnia generally experience high-quality, abundant resources, whereas lakes provide low-quality, seasonally shifting resources that are chronically limiting. For both ecotypes, we used replicate clones drawn from a number of separate populations. Fourteen genes were differentially regulated with respect to resources, including genes involved in gut processes, resource allocation, and activities with no obvious connection to resource exploitation. Three genes were differentially regulated in both ecotypes; the others may play a role in ecological divergence. Genes clearly linked to gut processes include two peritrophic matrix proteins, a Niemann-Pick type C2 gene, and a chymotrypsin. A pancreatic lipase, an epoxide hydrolase, a neuroparsin, and an UDP-dependent glucuronyltransferase are potentially involved in resource allocation through effects on energy processing and storage or hormone pathways. We performed quantitative rt-PCR for eight genes in independent samples of three clones of each of the two ecotypes. Though these largely confirmed observed differential regulation, some genes' expression was highly variable among clones. Our results demonstrate the value of matching the level of biological replication in genome-wide assays to the question, as it gave us insight into ecotype-level responses at ecological and evolutionary scales despite substantial variation within ecotypes.