[Show abstract][Hide abstract] ABSTRACT: Genes associated with the neurodevelopmental disorder microcephaly display a strong signature of adaptive evolution in primates. Comparative data suggest a link between selection on some of these loci and the evolution of primate brain size. Whether or not either positive selection or this phenotypic association are unique to primates is unclear, but recent studies in cetaceans suggest at least two microcephaly genes evolved adaptively in other large brained mammalian clades.
[Show abstract][Hide abstract] ABSTRACT: The Arctic skua (Stercorarius parasiticus) is a classic example of an avian plumage polymorphism, with variation in melanin-based ventral plumage coloration defining pale, intermediate and dark morphs in adults of both sexes. However, despite several decades of field research, there is an incomplete understanding of how the polymorphism in ventral plumage colour is maintained and the selective forces involved. Here, we investigate selection on a locus (MC1R) that is strongly associated with plumage colour variation in Arctic skuas using patterns of nucleotide variation and comparison to neutral loci (nuclear introns and mtDNA). We find that three linked nonsynonymous mutations in MC1R, including the single mutation described previously, are associated with plumage colour in the Arctic skua. The position of nonsynonymous mutations on a MC1R haplotype network implies that divergent selection drove the initial evolution of the colour morphs. Comparisons of FST s of MC1R vs. nuclear introns among five skua populations differing in proportion of dark morphs along an approximate north-south cline reveal a signature of divergent selection on MC1R. In contrast, we find limited evidence for balancing selection on MC1R within populations, although the power is low. Our results provide strong evidence for both past and ongoing selection on MC1R, and, by implication, plumage colour in Arctic skuas. The results suggest that a fruitful avenue for future ecological studies will be analysis of selection on morphs in colonies at the extremes along the morph ratio cline.
[Show abstract][Hide abstract] ABSTRACT: The Callitrichidae are the smallest anthropoids, whereas the Cheirogaleidae include the smallest of all primates. Using species-level analyses, we show that these are derived conditions; both neonatal and adult body mass decreased in a gradual, phyletic manner in parallel across callitrichids, and across cheirogaleids. We identify lineages with particularly rapid decreases and highlight the pygmy marmoset, Callithrix pygmaea, as a phenotypic outlier. The life-history traits associated with body-mass reduction in each clade suggest that the convergent evolution of small body size was achieved by changes in different ontogenetic stages. Body-size reduction in callitrichids appears to be almost exclusively due to alterations in prenatal growth rate, whereas body-size reduction in cheirogaleids may have been largely due to reduced duration of growth phases. Finally, we use these results to discuss some of the debates surrounding the evolution of Homo floresiensis and suggest potential parallels between the evolution of H. floresiensis and callitrichids.
Journal of Evolutionary Biology 02/2013; · 3.48 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Microcephaly genes are amongst the most intensively studied genes with candidate roles in brain evolution. Early controversies surrounded the suggestion that they experienced differential selection pressures in different human populations, but several association studies failed to find any link between variation in microcephaly genes and brain size in humans. Recently, however, sex-dependent associations were found between variation in three microcephaly genes and human brain size, suggesting that these genes could contribute to the evolution of sexually dimorphic traits in the brain. Here, we test the hypothesis that microcephaly genes contribute to the evolution of sexual dimorphism in brain mass across anthropoid primates using a comparative approach. The results suggest a link between selection pressures acting on MCPH1 and CENPJ and different scores of sexual dimorphism.
Journal of Evolutionary Biology 01/2013; · 3.48 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: AimTo investigate the intra‐specific genetic divergence and phenotypic diversification in Oophaga granulifera, analysing phylogeographical patterns, population structure, coloration and traits potentially involved in reproductive isolation. LocationCosta Rica. Methods
Our phylogeographical analysis used the mitochondrial genes cytochrome b and 16S. We sequenced the two markers in 28 individuals belonging to 10 populations and 16 individuals from nine populations, respectively. The population structure was analysed based on seven polymorphic microsatellite loci in 7–15 individuals from 11 populations using maximum likelihood and Bayesian analyses. The colour phenotypes of 189 frogs and the reflectance spectra of 15 frogs from five populations were measured. In nine populations, we recorded the advertisement calls of 59 males and measured 10 morphological variables from 147 frogs. ResultsOur phylogeographical reconstruction supported the divergence into southern and northern lineages in O. granulifera. In a colour transition area between the main red and green morphs, we describe novel gradual intermediate phenotypes occurring in polymorphic populations. The colour distribution was asymmetrical compared to the genetic variation: the southern lineage included only monomorphic red populations while the northern lineage contained red, green and polymorphic populations. The two lineages differed significantly in advertisement calls and morphology. Microsatellites confirmed the clear inter‐lineage divergence. In the northern lineage, the red morph differed from the intermediate and green morphs in the pulse rate of the advertisement call and in body size. In the colour transition area, there was no simple genetic or colour cline. Main conclusionsOophaga granulifera has evolved into two genetic lineages. The reduced gene flow and diversification in advertisement calls and morphology point to reproductive isolation between lineages. Within the northern lineage, the presence of gradual intermediate morphs and the population structure support the presence of gene flow across the colour transition area while the red versus intermediate–green divergence in both calls and morphology reveals the potential for assortative mating. Our data all congruently show that O. granulifera presents deep intra‐specific divergence. The lack of genetic diversification among colour morphs and the genetic connectivity among the populations defining the colour transition area suggest that the colour diversification in the species is a recent phenomenon.
Journal of Biogeography 01/2013; 40(2). · 4.86 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Two classes of vomeronasal receptor genes, V1R and V2R, occur in vertebrates. Whereas, V1R loci are found in a wide variety of mammals, including primates, intact V2R genes have thus far only been described in rodents and marsupials. In primates, the V2R repertoire has been considered degenerate. Here, we identify for the first time two intact V2R loci in a strepsirrhine primate, the grey mouse lemur (Microcebus murinus), and demonstrate their expression in the vomeronasal organ. Putatively functional orthologues are present in two other strepsirrhines, whereas, both loci are pseudogenes in a range of anthropoid species. The functional significance of the loci is unknown, but positive selection on one of them is consistent with an adaptive role in pheromone detection. Finally, conservation of V2R loci in strepsirrhines is notable, given their high diversity and role in MUP and MHC detection in rodents.
[Show abstract][Hide abstract] ABSTRACT: A fundamental principle of Batesian mimicry is that it pays to look like a local harmful species that is recognizable to other local species (receivers). Mimicking an allopatric species confers no benefit, as it is not recognizable to local species. It is thought that the common cuckoo, Cuculus canorus, is a Batesian mimic of the Eurasian sparrowhawk, Accipiter nisus, predominantly via its barred plumage, which facilitates access to host nests to deposit eggs. Barring is widespread in five genera of Old World cuckoos, unlike nonparasitic cuckoos, and evolved after the evolution of parasitism. Although barred plumage is predominant in parasitic cuckoos, it is unclear whether it may have a widespread function in cuckoo–hawk mimicry. If widespread, there should be a visual similarity between all five genera of Old World parasitic cuckoos and sympatric raptors. In addition, given that it pays to look like a local harmful species, sympatry should predict the degree of similarity. We compared barred plumage from all five genera of parasitic Old World cuckoos and up to eight sympatric raptors using digital image analysis. Cuckoos predominantly matched most raptors for at least one pattern attribute. In addition, three out of five cuckoos closely resembled a sympatric raptor for all barred pattern attributes examined, and potential model species were not confined to sparrowhawks. Habitat did not appear to influence plumage pattern similarity in most species studied. Finally, the barred plumage of sympatric species was more similar in appearance than those in allopatry. Together this demonstrates that cuckoos look like a local harmful species, which is congruous with Batesian mimicry.
[Show abstract][Hide abstract] ABSTRACT: Variation in substitution rates across a phylogeny can be indicative of shifts in the evolutionary dynamics of a protein or non-protein coding regions. One way to understand these signals is to seek the phenotypic correlates of rate variation. Here, we extended a previously published likelihood method designed to detect evolutionary associations between genotypic evolutionary rate and phenotype over a phylogeny. In simulation with two discrete categories of phenotype, the method has a low false-positive rate and detects greater than 80% of true-positives with a tree length of three or greater and a three-fold or greater change in substitution rate given the phenotype. In addition, we successfully extend the test from two to four phenotype categories and evaluated its performance. We then applied the method to two major hypotheses for rate variation in the mitochondrial genome of primates-longevity and generation time as well as body mass which is correlated with many aspects of life history-using three categories of phenotype through discretization of continuous values. Similar to previous results for mammals, we find that the majority of mitochondrial protein-coding genes show associations consistent with the longevity and body mass predictions and that the predominant signal of association comes from the third codon position. We also found a significant association between maximum lifespan and the evolutionary rate of the control region of the mtDNA. In contrast, 24 protein-coding genes from the nuclear genome do not show a consistent pattern of association, which is inconsistent with the generation time hypothesis. These results show the extended method can robustly identify genotype-phenotype associations up to at least four phenotypic categories, and demonstrate the successful application of the method to study factors affecting neutral evolutionary rate in protein-coding and non-coding loci.
[Show abstract][Hide abstract] ABSTRACT: A long-held dogma in comparative neurobiology has been that the number of neurons under a given area of cortical surface is constant. As such, the attention of those seeking to understand the genetic basis of brain evolution has focused on genes with functions in the lateral expansion of the developing cerebral cortex. However, new data suggest that cortical cytoarchitecture is not constant across primates, raising the possibility that changes in radial cortical development played a role in primate brain evolution. We present the first analysis of a gene with functions relevant to this dimension of brain evolution. We show that NIN, a gene necessary for maintaining asymmetric, neurogenic divisions of radial glial cells (RGCs), evolved adaptively during anthropoid evolution. We explored how this selection relates to neural phenotypes and find a significant association between selection on NIN and neonatal brain size in catarrhines. Our analyses suggest a relationship with prenatal neurogenesis and identify the human data point as an outlier, possibly explained by postnatal changes in development on the human lineage. A similar pattern is found in platyrrhines, but the highly encephalized genus Cebus departs from the general trend. We further show that the evolution of NIN may be associated with variation in neuron number not explained by increases in surface area, a result consistent with NIN's role in neurogenic divisions of RGCs. Our combined results suggest a role for NIN in the evolution of cortical development.
Genes Brain and Behavior 08/2012; · 3.60 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Chemosensory genes are frequently the target of positive selection and are often present in large gene families, but little is known about heterogeneity of selection in these cases and its relation to function. Here, we use the vomeronasal-1 receptor (V1R) repertoire of mouse lemurs (Microcebus spp.) as a model system to study patterns of selection of chemosensory genes at several different levels. Mouse lemurs are small nocturnal strepsirrhine primates and have a large (∼200 loci) repertoire of V1R loci that are likely important for intraspecific pheromonal communication and interspecific interactions, for example, recognition of predator cues. We investigated signals and patterns of positive selection among the 105 identified full length V1R loci in the gray mouse lemur and within 7 V1R loci amplified across multiple mouse lemur species. Phylogenetic reconstructions of published sequences revealed at least nine monophyletic clusters of V1Rs in gray mouse lemurs that have diversified since the split between lemurs and lorisoid primates. A large majority of clusters evolved under significant positive selection. Similar results were found in V1Rs of closely related greater galagos. Comparison with function of related V1R clusters in mice suggested a potential relationship between receptor function and strength of selection. Interestingly, most codons identified as being under positive selection are located in the extracellular domains of the receptors and hence likely indicate the position of residues involved in ligand binding. Positive selection was also detected within five V1R loci (=71% of analyzed loci) sequenced from 6 to 10 mouse lemur species, indicating ongoing selection within the genus, which may be related to sexual selection and, potentially, speciation processes. Variation in strength of positive selection on V1Rs showed no simple relationship to cluster size. The diversity of V1R loci in mouse lemurs reflects their adaptive evolution and is most likely related to the fundamental relevance of olfactory communication and predator recognition in these primates. Overall, adaptive evolution is the predominant mode of evolution of V1R loci at all levels, and the substantial heterogeneity in the strength of selection may be related to receptor function.
Molecular Biology and Evolution 07/2012; 29:3807-. · 10.35 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: When simple sequence repeats are integrated into functional genes, they can potentially act as evolutionary 'tuning knobs', supplying abundant genetic variation with minimal risk of pleiotropic deleterious effects. The genetic basis of variation in facial shape and length represents a possible example of this phenomenon. Runt-related transcription factor 2 (RUNX2), which is involved in osteoblast differentiation, contains a functionally-important tandem repeat of glutamine and alanine amino acids. The ratio of glutamines to alanines (the QA ratio) in this protein seemingly influences the regulation of bone development. Notably, in domestic breeds of dog, and in carnivorans in general, the ratio of glutamines to alanines is strongly correlated with facial length.
In this study we examine whether this correlation holds true across placental mammals, particularly those mammals for which facial length is highly variable and related to adaptive behavior and lifestyle (e.g., primates, afrotherians, xenarthrans). We obtained relative facial length measurements and RUNX2 sequences for 41 mammalian species representing 12 orders. Using both a phylogenetic generalized least squares model and a recently-developed Bayesian comparative method, we tested for a correlation between genetic and morphometric data while controlling for phylogeny, evolutionary rates, and divergence times. Non-carnivoran taxa generally had substantially lower glutamine-alanine ratios than carnivorans (primates and xenarthrans with means of 1.34 and 1.25, respectively, compared to a mean of 3.1 for carnivorans), and we found no correlation between RUNX2 sequence and face length across placental mammals.
Results of our diverse comparative phylogenetic analyses indicate that QA ratio does not consistently correlate with face length across the 41 mammalian taxa considered. Thus, although RUNX2 might function as a 'tuning knob' modifying face length in carnivorans, this relationship is not conserved across mammals in general.
[Show abstract][Hide abstract] ABSTRACT: Gorillas are humans' closest living relatives after chimpanzees, and are of comparable importance for the study of human origins and evolution. Here we present the assembly and analysis of a genome sequence for the western lowland gorilla, and compare the whole genomes of all extant great ape genera. We propose a synthesis of genetic and fossil evidence consistent with placing the human-chimpanzee and human-chimpanzee-gorilla speciation events at approximately 6 and 10 million years ago. In 30% of the genome, gorilla is closer to human or chimpanzee than the latter are to each other; this is rarer around coding genes, indicating pervasive selection throughout great ape evolution, and has functional consequences in gene expression. A comparison of protein coding genes reveals approximately 500 genes showing accelerated evolution on each of the gorilla, human and chimpanzee lineages, and evidence for parallel acceleration, particularly of genes involved in hearing. We also compare the western and eastern gorilla species, estimating an average sequence divergence time 1.75 million years ago, but with evidence for more recent genetic exchange and a population bottleneck in the eastern species. The use of the genome sequence in these and future analyses will promote a deeper understanding of great ape biology and evolution.
[Show abstract][Hide abstract] ABSTRACT: In spite of its evolutionary significance and conservation importance, the population structure of the common chimpanzee, Pan troglodytes, is still poorly understood. An issue of particular controversy is whether the proposed fourth subspecies of chimpanzee, Pan troglodytes ellioti, from parts of Nigeria and Cameroon, is genetically distinct. Although modern high-throughput SNP genotyping has had a major impact on our understanding of human population structure and demographic history, its application to ecological, demographic, or conservation questions in non-human species has been extremely limited. Here we apply these tools to chimpanzee population structure, using ∼700 autosomal SNPs derived from chimpanzee genomic data and a further ∼100 SNPs from targeted re-sequencing. We demonstrate conclusively the existence of P. t. ellioti as a genetically distinct subgroup. We show that there is clear differentiation between the verus, troglodytes, and ellioti populations at the SNP and haplotype level, on a scale that is greater than that separating continental human populations. Further, we show that only a small set of SNPs (10-20) is needed to successfully assign individuals to these populations. Tellingly, use of only mitochondrial DNA variation to classify individuals is erroneous in 4 of 54 cases, reinforcing the dangers of basing demographic inference on a single locus and implying that the demographic history of the species is more complicated than that suggested analyses based solely on mtDNA. In this study we demonstrate the feasibility of developing economical and robust tests of individual chimpanzee origin as well as in-depth studies of population structure. These findings have important implications for conservation strategies and our understanding of the evolution of chimpanzees. They also act as a proof-of-principle for the use of cheap high-throughput genomic methods for ecological questions.
[Show abstract][Hide abstract] ABSTRACT: A fundamental trend during primate evolution has been the expansion of brain size. However, this trend was reversed in the Callitrichidae (marmosets and tamarins), which have secondarily evolved smaller brains associated with a reduction in body size. The recent pursuit of the genetic basis of brain size evolution has largely focused on episodes of brain expansion, but new insights may be gained by investigating episodes of brain size reduction. Previous results suggest two genes (ASPM and CDK5RAP2) associated with microcephaly, a human neurodevelopmental disorder, may have an evolutionary function in primate brain expansion. Here we use new sequences encoding key functional domains from 12 species of callitrichids to show that positive selection has acted on ASPM across callitrichid evolution and the rate of ASPM evolution is significantly negatively correlated with callitrichid brain size, whereas the evolution of CDK5RAP2 shows no correlation with brain size. Our findings strongly suggest that ASPM has a previously unsuspected role in the evolution of small brains in primates. ASPM is therefore intimately linked to both evolutionary increases and decreases in brain size in anthropoids and is a key target for natural selection acting on brain size.
[Show abstract][Hide abstract] ABSTRACT: Highlights
► Colour vision status of captive and wild tamarins (Saguinus) affects insect capture. ► Trichromats catch more prey than dichromats, but prey size does not differ. ► Dichromats catch a higher proportion of camouflaged prey than trichromats. ► Heterozygote advantage may help maintain the genetic polymorphism of colour vision. ► Frequency-dependent selection on colour vision phenotypes may also play a role.
[Show abstract][Hide abstract] ABSTRACT: Carotenoid-based colour signals are widespread in the animal kingdom and common textbook examples of sexually selected traits. Carotenoid pigments must be obtained through the diet as all animals lack the enzymatic machinery necessary to synthesize them from scratch. Once ingested, carotenoids are metabolized, stored, transported and deposited, and some or all of these processes may be limiting for signal production and thus subjected to social or sexual selection on phenotypic coloration. Very little is known about which genes and physiological pathways are involved in carotenoid pigmentation which is unfortunate, as genetic information would allow us to investigate the biochemical consequences of sexual selection. In this study, we present a transcriptome-screening technique and apply it to a carotenoid-signalling bird species, the southern red bishop Euplectes orix, to uncover the gene(s) responsible for the conversion of dietary β-carotene (orange) to canthaxanthin (bright red). The transcriptome, extracted from the liver of a male entering his breeding moult, is expressed within bacterial cells genetically modified to synthesize beta-carotene. Effects of expressed E. orix proteins on the structure or amount of β-carotene are initially detected by eye (based on colour change) and subsequently confirmed by high-performance liquid chromatography. Here, we demonstrate the validity of the technique and provide a list of candidate genes involved in the carotenoid pigmentation pathway. We believe that this method could be applied to other species and tissues and that this may help researchers uncover the genetic basis of carotenoid coloration in vertebrates.
[Show abstract][Hide abstract] ABSTRACT: Carotenoid-based coloration has attracted much attention in evolutionary biology owing to its role in honest, condition-dependent signalling. Knowledge of the genetic pathways that regulate carotenoid coloration is crucial for an understanding of any trade-offs involved. We identified genes with potential roles in carotenoid coloration in vertebrates via (i) carotenoid uptake (SR-BI, CD36), (ii) binding and deposition (StAR1, MLN64, StAR4, StAR5, APOD, PLIN, GSTA2), and (iii) breakdown (BCO2, BCMO1). We examined the expression of these candidate loci in carotenoid-coloured tissues and several control tissues of the red-billed quelea (Quelea quelea), a species that exhibits a male breeding plumage colour polymorphism and sexually dimorphic variation in bill colour. All of the candidate genes except StAR1 were expressed in both the plumage and bill of queleas, indicating a potential role in carotenoid coloration in the quelea. However, no differences in the relative expression of any of the genes were found among the quelea carotenoid phenotypes, suggesting that other genes control the polymorphic and sexually dimorphic variation in carotenoid coloration observed in this species. Our identification of a number of potential carotenoid genes in different functional categories provides a critical starting point for future work on carotenoid colour regulation in vertebrate taxa.
Proceedings of the Royal Society B: Biological Sciences 05/2011; 279(1726):58-66. · 5.68 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The anatomical basis and adaptive function of the expansion in primate brain size have long been studied; however, we are only beginning to understand the genetic basis of these evolutionary changes. Genes linked to human primary microcephaly have received much attention as they have accelerated evolutionary rates along lineages leading to humans. However, these studies focus narrowly on apes, and the link between microcephaly gene evolution and brain evolution is disputed. We analyzed the molecular evolution of four genes associated with microcephaly (ASPM, CDK5RAP2, CENPJ, MCPH1) across 21 species representing all major clades of anthropoid primates. Contrary to prevailing assumptions, positive selection was not limited to or intensified along the lineage leading to humans. In fact we show that all four loci were subject to positive selection across the anthropoid primate phylogeny. We developed clearly defined hypotheses to explicitly test if selection on these loci was associated with the evolution of brain size. We found positive relationships between both CDK5RAP2 and ASPM and neonatal brain mass and somewhat weaker relationships between these genes and adult brain size. In contrast, there is no evidence linking CENPJ and MCPH1 to brain size evolution. The stronger association of ASPM and CDK5RAP2 evolution with neonatal brain size than with adult brain size is consistent with these loci having a direct effect on prenatal neuronal proliferation. These results suggest that primate brain size may have at least a partially conserved genetic basis. Our results contradict a previous study that linked adaptive evolution of ASPM to changes in relative cortex size; however, our analysis indicates that this conclusion is not robust. Our finding that the coding regions of two widely expressed loci has experienced pervasive positive selection in relation to a complex, quantitative developmental phenotype provides a notable counterexample to the commonly asserted hypothesis that cis-regulatory regions play a dominant role in phenotypic evolution.
Molecular Biology and Evolution 10/2010; 28(1):625-38. · 10.35 Impact Factor