Development of foraging skills in two orangutan populations: needing to learn or needing to grow?

Background

Orangutans have one of the slowest-paced life histories of all mammals. Whereas life-history theory suggests that the time to reach adulthood is constrained by the time needed to reach adult body size, the needing-to-learn hypothesis instead suggests that it is limited by the time needed to acquire adult-level skills.To test between these two hypotheses, we compared the development of foraging skills and growth trajectories of immature wild orangutans in two populations: at Tuanan (Pongo pygmaeus wurmbii), Borneo, and Suaq Balimbing (Pongo abelii), Sumatra. We collected behavioral data on diet repertoire, feeding rates and ranging competence during focal follows, and estimated growth through non-invasive laser photogrammetry.

Results

We found that adult-like diet repertoires are attained around the age of weaning and that female immatures increase their repertoire size faster than their male peers. Adult-level feeding rates of easy techniques are reached just after weaning, but several years later for more difficult techniques, albeit always before adulthood (i.e. age at first reproduction). Independent immatures had faster feeding rates for easy to process items than their mothers, with male immatures achieving faster feeding rates earlier in development relative to females. Sumatran immatures reach adult-level feeding rates 2–3 years later than their Bornean peers, in line with their higher dietary complexity and later weaning. The range-use competence of independently ranging and weaned immatures is similar to that of adult females. Body size measurements showed, immatures grow until female age of first reproduction.

Conclusions

In conclusion, unlike in humans, orangutan foraging skills are in place prior to reproduction. Growth trajectories suggest that energetic constraints, rather than skills, best explain the length of immaturity. However, skill competence for dietary independence is reached later where the adult niche is more complex, which is consistent with the relatively later weaning age with increasing brain size found generally in primates, and apes in particular.

     

Odontocete occurrence in relation to changes in oceanography at a remote equatorial Pacific seamount

Seamounts are considered hot spots of biodiversity and can aggregate pelagic predators and their prey. Passive acoustic monitoring was conducted over 3 mo in 2012 to document the occurrence of odontocetes near a seamount chain in the central equatorial Pacific in relation to oceanographic changes over time. Beaked whale echolocation signals were most frequently encountered. The main beaked whale signal was an unknown type, BW38, which resembled signals produced by Blainville's beaked whales. It had high occurrence during high sea surface temperature and low sea surface salinity. Cuvier's beaked whales were the second most detected. They had an opposite pattern and were encountered more often when sea surface temperature was low and net primary productivity was high. Risso's dolphins and short‐finned pilot whales had high acoustic densities, and echolocated predominantly at night. Risso's dolphins occurred more often during low sea surface height deviation. False killer whales were less frequently detected and mostly occurred during the day. Sperm whale detections were fewer than expected and associated with high chlorophyll a. Short duration Kogiidae encounters occurred on average every third day. These types of long‐term site studies are an informative tool to comparatively assess species composition, relative abundance, and relationship to oceanographic changes.     

Therapeutic efficacy of anti‐MMP9 antibody in combination with nab‐paclitaxel‐based chemotherapy in pre‐clinical models of pancreatic cancer

Matrix metalloproteinase 9 (MMP9) is involved in the proteolysis of extracellular proteins and plays a critical role in pancreatic ductal adenocarcinoma (PDAC) progression, invasion and metastasis. The therapeutic potential of an anti‐MMP9 antibody (αMMP9) was evaluated in combination with nab‐paclitaxel (NPT)‐based standard cytotoxic therapy in pre‐clinical models of PDAC. Tumour progression and survival studies were performed in NOD/SCID mice. The mechanistic evaluation involved RNA‐Seq, Luminex, IHC and Immunoblot analyses of tumour samples. Median animal survival compared to controls was significantly increased after 2‐week therapy with NPT (59%), Gem (29%) and NPT+Gem (76%). Addition of αMMP9 antibody exhibited further extension in survival: NPT+αMMP9 (76%), Gem+αMMP9 (47%) and NPT+Gem+αMMP9 (94%). Six‐week maintenance therapy revealed that median animal survival was significantly increased after NPT+Gem (186%) and further improved by the addition of αMMP9 antibody (218%). Qualitative assessment of mice exhibited that αMMP9 therapy led to a reduction in jaundice, bloody ascites and metastatic burden. Anti‐MMP9 antibody increased the levels of tumour‐associated IL‐28 (1.5‐fold) and decreased stromal markers (collagen I, αSMA) and the EMT marker vimentin. Subcutaneous tumours revealed low but detectable levels of MMP9 in all therapy groups but no difference in MMP9 expression. Anti‐MMP9 antibody monotherapy resulted in more gene expression changes in the mouse stroma compared to the human tumour compartment. These findings suggest that anti‐MMP9 antibody can exert specific stroma‐directed effects that could be exploited in combination with currently used cytotoxics to improve clinical PDAC therapy.     

Effects of nutrient limitation on sperm and seminal fluid: a systematic review and meta‐analysis

Theory predicts that costly sexual traits should be reduced when individuals are in poor condition (i.e. traits should exhibit condition‐dependent expression). It is therefore widely expected that male ejaculate traits, such as sperm and seminal fluid, will exhibit reduced quantity and quality when dietary nutrients are limited. However, reported patterns of ejaculate condition dependence are highly variable, and there has been no comprehensive synthesis of underlying sources of such variation in condition‐dependent responses. In particular, it remains unclear whether all ejaculate traits are equally sensitive to nutrient intake, and whether such traits are particularly sensitive to certain dietary nutrients, respond more strongly to nutrients during specific life stages, or respond more strongly in some taxonomic groups. We systematically reviewed these potential sources of variation through a meta‐analysis across 50 species of arthropods and vertebrates (from 71 papers and 348 effect sizes). We found that overall, ejaculate traits are moderately reduced when dietary nutrients are limited, but we also detected substantial variation in responses. Seminal fluid quantity was strongly and consistently condition dependent, while sperm quantity was moderately condition dependent. By contrast, aspects of sperm quality (particularly sperm viability and morphology) were less consistently reduced under nutrient limitation. Ejaculate traits tended to respond in a condition‐dependent manner to a wide range of dietary manipulations, especially to caloric and protein restriction. Finally, while all major taxa for which sufficient data exist (i.e. arthropods, mammals, fish) showed condition dependence of ejaculate traits, we detected some taxonomic differences in the life stage that is most sensitive to nutrient limitation, and in the degree of condition dependence of specific ejaculate traits. Together, these biologically relevant factors accounted for nearly 20% of the total variance in ejaculate responses to nutrient limitation. Interestingly, body size showed considerably stronger condition‐dependent responses compared to ejaculate traits, suggesting that ejaculate trait expression may be strongly canalised to protect important reproductive functions, or that the cost of producing an ejaculate is relatively low. Taken together, our findings show that condition‐dependence of ejaculate traits is taxonomically widespread, but there are also many interesting, biologically relevant sources of variation that require further investigation. In particular, further research is needed to understand the differences in selective pressures that result in differential patterns of ejaculate condition dependence across taxa and ejaculate traits.     

Microbial diversity of an Antarctic subglacial community and high-resolution replicate sampling inform hydrological connectivity in a polar desert

Antarctic subglacial environments host microbial ecosystems and are proving to be geochemically and biologically diverse. The Taylor Glacier, Antarctica, periodically expels iron-rich brine through a conduit sourced from a deep subglacial aquifer, creating a dramatic red surface feature known as Blood Falls. We used Illumina MiSeq sequencing to describe the core microbiome of this subglacial brine and identified previously undetected but abundant groups including the candidate bacterial phylum Atribacteria and archaeal phylum Pacearchaeota. Our work represents the first microbial characterization of samples collected from within a glacier using a melt probe, and the only Antarctic subglacial aquatic environment that, to date, has been sampled twice. A comparative analysis showed the brine community to be stable at the operational taxonomic unit level of 99% identity over a decade. Higher resolution sequencing enabled deconvolution of the microbiome of subglacial brine from mixtures of materials collected at the glacier surface. Diversity patterns between this brine and samples from the surrounding landscape provide insight into the hydrological connectivity of subglacial fluids to the surface polar desert environment. Understanding subice brines collected on the surfaces of thick ice covers has implications for analyses of expelled materials that may be sampled on icy extraterrestrial worlds.     

Estimating the impact of divergent mating phenology between residents and migrants on the potential for gene flow

Gene flow between populations can allow the spread of beneficial alleles and genetic diversity between populations, with importance to conservation, invasion biology, and agriculture. Levels of gene flow between populations vary not only with distance, but also with divergence in reproductive phenology. Since phenology is often locally adapted, arriving migrants may be reproductively out of synch with residents, which can depress realized gene flow. In flowering plants, the potential impact of phenological divergence on hybridization between populations can be predicted from overlap in flowering schedules—the daily count of flowers capable of pollen exchange—between a resident and migrant population. The accuracy of this prospective hybridization estimate, based on parental phenotypes, rests upon the assumptions of unbiased pollen transfer between resident and migrant active flowers. We tested the impact of phenological divergence on resident–migrant mating frequencies in experiments that mimicked a single large gene flow event. We first prospectively estimated mating frequencies two lines of Brassica rapaselected or early and late flowering. We then estimated realized mating frequencies retrospectively through progeny testing. The two estimates strongly agreed in a greenhouse experiment, where procedures ensured saturating, unbiased pollination. Under natural pollination in the field, the rate of resident–migrant mating, was lower than estimated by phenological divergence alone, although prospective and retrospective estimates were correlated. In both experiments, differences between residents and migrants in flowering schedule shape led to asymmetric hybridization. Results suggest that a prospective estimate of hybridization based on mating schedules can be a useful, although imperfect, tool for evaluating potential gene flow. They also illustrate the impact of mating phenology on the magnitude and symmetry of reproductive isolation.     

Labeling, detection and identification of newly synthesized proteomes with bioorthogonal non-canonical amino-acid tagging

A major aim of proteomics is the identification of proteins in a given proteome at a given metabolic state. This protocol describes the step-by-step labeling, purification and detection of newly synthesized proteins in mammalian cells using the non-canonical amino acid azidohomoalanine (AHA). In this method, metabolic labeling of newly synthesized proteins with AHA endows them with the unique chemical functionality of the azide group. In the subsequent click chemistry tagging reaction, azide-labeled proteins are covalently coupled to an alkyne-bearing affinity tag. After avidin-based affinity purification and on-resin trypsinization, the resulting peptide mixture is subjected to tandem mass spectrometry for identification. In combination with deuterated leucine-based metabolic colabeling, candidate proteins can be immediately validated. Bioorthogonal non-canonical amino-acid tagging can be combined with any subcellular fractionation, immunopurification or other proteomic method to identify specific subproteomes, thereby reducing sample complexity and enabling the identification of subtle changes in a proteome. This protocol can be completed in 5 days.