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Bradley, B. J.

Publications and source records attributed to Bradley, B. J..

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Melanism in a wild sifaka population: Darker where cold and fragmented

Pigmentation is one of the most striking examples of diversity in the natural world. Mainly, pelage (hair/fur) pigmentation provides a substrate for selection (i.e., crypsis, signaling, thermoregulation) and is capable of rapid change. Thus, this trait may be the one potential early signal of adaptation (or maladaptation) in wild primate populations. However, most of our hypotheses on the forces responsible for primate pelage pigmentation are based solely on macro-evolutionary studies. Here, we characterize pelage color and pattern variation within a population of wild primates, diademed sifakas (Propithecus diadema), exhibiting striking diversity in coloration (melanic to tri-colored). Our approach jointly assesses climate and pelage variation across the region. We score pelage using a semi-quantitative methodology. We then test if pelage variation is associated with climatic or demographic factors (i.e., sex-class, age-class) across the Tsinjoarivo forest, Madagascar. We find darker bodies and less complex faces occur in colder and more fragmented forests. We explore three hypotheses that may explain this phenotypic pattern: isolation by distance, an environmental gradient, or unique local adaptation. Importantly, each scenario signals the need for enhanced conservation of diademed sifakas in the Tsinjoarivo forest. More studies on primate pigmentation in wild populations will be needed to contextualize if this pattern is exceptional or typical. It is likely that in other primate populations pigmentation may also foretell of adaptation or environmental mismatch.

evolutionary biology↗

Hair phenotype diversity across Indriidae lemurs

ObjectivesHair (i.e., pelage/fur) is a salient feature of primate (including human) diversity and evolution-- serving functions tied to thermoregulation, protection, camouflage, and signaling--but wild primate pelage evolution remains relatively understudied. Specifically, assessing multiple hypotheses across distinct phylogenetic scales is essential but is rarely conducted. We examine whole body hair color and density variation across Indriidae (Avahi, Indri, Propithecus)--a lineage that, like humans, exhibits vertical posture (i.e., their whole bodies are vertical to the sun). Materials and MethodsOur analyses consider multiple phylogenetic scales (family-level, genus-level) and hypotheses (e.g., Glogers rule, the body cooling hypotheses). We obtain hair color and density from museum and/or wild animals, opsin genotypes from wild animals, and climate data from WorldClim. To analyze our data, we use phylogenetic generalized linear mixed models (PGLMM) using Markov chain Monte Carlo algorithms. ResultsOur results show that across the Indriidae family, darker hair is typical in wetter regions. However, within Propithecus, dark black hair is common in colder forest regions. Results also show pelage redness increases in populations exhibiting enhanced color vision. Lastly, we find follicle density on the crown and limbs increases in dry and open environments. DiscussionThis study highlights how different selective pressures across distinct phylogenetic scales have likely acted on primate hair evolution. Specifically, our data across Propithecus may implicate thermoregulation and is the first empirical evidence of Bogerts rule in mammals. Our study also provides rare empirical evidence supporting an early hypothesis on hominin hair evolution.

evolutionary biology↗

Molecular adaptation to folivory and the conservation implications for Madagascar's lemurs

Folivory evolved independently at least three times over the last 40 million years among Madagascars lemurs. Many extant lemuriform folivores exist in sympatry in Madagascars remaining forests. These species avoid feeding competition by adopting different dietary strategies within folivory, reflected in behavioral, morphological, and microbiota diversity across species. These conditions make lemurs an ideal study system for understanding adaptation to leaf-eating. Most folivorous lemurs are also highly endangered. The significance of folivory for conservation outlook is complex. Though generalist folivores may be relatively well equipped to survive habitat disturbance, specialist folivores occupying narrow dietary niches may be less resilient. Characterizing the genetic bases of adaptation to folivory across species and lineages can provide insights into their differential physiology and potential to resist habitat change. We recently reported accelerated genetic change in RNASE1, a gene encoding an enzyme (RNase 1) involved in molecular adaptation in mammalian folivores, including various monkeys and sifakas (genus Propithecus; family Indriidae). Here, we sought to assess whether other lemurs, including phylogenetically and ecologically diverse folivores, might show parallel adaptive change in RNASE1 that could underlie a capacity for efficient folivory. We characterized RNASE1 in 21 lemur species representing all five families and members of the three extant folivorous lineages: 1) bamboo lemurs (family Lemuridae), 2) sportive lemurs (family Lepilemuridae), and 3) indriids (family Indriidae). We found pervasive sequence change in RNASE1 across all indriids, a dN/dS value > 3 in this clade, and evidence for shared change in isoelectric point, indicating altered enzymatic function. Sportive and bamboo lemurs, in contrast, showed more modest sequence change. The greater change in indriids may reflect a shared strategy emphasizing complex gut morphology and microbiota to facilitate folivory. This case study illustrates how genetic analysis may reveal differences in functional traits that could influence species ecology and, in turn, their resilience to habitat change. Moreover, our results support the contention that not all primate folivores are built the same and highlight the need to avoid generalizations about dietary guild in considering conservation outlook, particularly in lemurs where such diversity in folivory has probably led to extensive specialization via niche partitioning.

ecology↗

Genetic relatedness cannot explain social bonds in black-and-white ruffed lemurs (Varecia variegata).

Fission-fusion social dynamics are common among a number of vertebrate taxa, and yet the factors shaping these variable associations among subgroup members have not been widely addressed. Associations may occur simply because of shared habitat preferences; however, social ties may also be influenced by genetic relatedness (kinship) or social attraction. Here, we investigate the association patterns of wild black-and-white ruffed lemurs, Varecia variegata, in Ranomafana National Park, Madagascar using behavioural, spatial (home range), and genetic data from twenty-four individually identified animals. We collected 40,840 records of group composition over a 17-month period and from this calculated pairwise association indices. We also used ranging coordinates and genetic samples to estimate patterns of spatial overlap and kinship, and then related these measures to patterns of affiliation. From these analyses, we found that dyadic ruffed lemur social associations were generally sparse and weak; that home range overlap was minimal; and that average relatedness within the community was low. We found no evidence that kinship was related to patterns of either spatial overlap or social association; instead, associations were primarily driven by space use. Moreover, social preferences were unrelated to kinship. While home range overlap explained most of the variation seen in social association, some variation remains unaccounted for, suggesting that other social, ecological, and biological factors such as shared resource defense or communal breeding might also play a role in social attraction. Our results further highlight the need to consider individual space use and nuances of species behavior when investigating social preference and social association more generally.

animal behavior and cognition↗

Successful exome capture and sequencing in lemurs using human baits

ObjectivesWe assessed the efficacy of exome capture in lemurs using commercially available human baits.\n\nMaterials and MethodsWe used two human kits (Nimblegen SeqCap EZ Exome Probes v2.0; IDT xGen Exome Research Panel v1.0) to capture and sequence the exomes of wild Verreauxs sifakas (Propithecus verreauxi, n = 8), a lemur species distantly related to humans. For comparison, we also captured exomes of a primate species more closely related to humans (Macaca mulatta, n= 4). We mapped reads to both the human reference assembly and the most closely related reference for each species before calling variants. We used measures of mapping quality and read coverage to compare capture success.\n\nResultsWe observed high and comparable mapping qualities for both species when mapped to their respective nearest-relative reference genomes. When investigating breadth of coverage, we found greater capture success in macaques than sifakas using both nearest-relative and human assemblies. Exome capture in sifakas was still highly successful with more than 90% of annotated coding sequence in the sifaka reference genome captured, and 80% sequenced to a depth greater than 7x using Nimblegen baits. However, this success depended on probe design: the use of IDT probes resulted in substantially less callable sequence at low-to-moderate depths.\n\nDiscussionOverall, we demonstrate successful exome capture in lemurs using human baits, though success differed between kits tested. These results indicate that exome capture is an effective and economical genomic method of broad utility to evolutionary primatologists working across the entire primate order.

genomics↗