Novel opsin gene variation in large-bodied, diurnal lemurs

Some primate populations include both trichromatic and dichromatic (red-green colour blind) individuals due to allelic variation at the X-linked opsin locus. This polymorphic trichromacy is well described in day-active New World monkeys. Less is known about colour vision in Malagasy lemurs, but, unlike New World monkeys, only some day-active lemurs are polymorphic, while others are dichromatic. The evolutionary pressures underlying these differences in lemurs are unknown, but aspects of species ecology, including variation in activity pattern, are hypothesized to play a role. Limited data on X-linked opsin variation in lemurs make such hypotheses difficult to evaluate. We provide the first detailed examination of X-linked opsin variation across a lemur clade (Indriidae). We sequenced the X-linked opsin in the most strictly diurnal and largest extant lemur, Indri indri, and nine species of smaller, generally diurnal indriids (Propithecus). Although nocturnal Avahi (sister taxon to Propithecus) lacks a polymorphism, at least eight species of diurnal indriids have two or more X-linked opsin alleles. Four rainforest-living taxa-I. indri and the three largest Propithecus species-have alleles not previously documented in lemurs. Moreover, we identified at least three opsin alleles in Indri with peak spectral sensitivities similar to some New World monkeys

Genomic Tools for Evolution and Conservation in the Chimpanzee: Pan troglodytes ellioti Is a Genetically Distinct Population

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

Estimates of the proportion of the sampled genomic regions for which the most closely related haplotype comes from each study population, for chimpanzees and humans.

<p>Parentheses show the empirical central 95% region of the distribution of values for the 100 re-samples of the human data.</p

Map of the geographic distribution of four populations of common chimpanzee.

<p><i>After </i><a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002504#pgen.1002504-Gonder2" target="_blank">[<i>3</i>]</a><i>, Figure 6b</i>. Colours show the ranges of each population (yellow - <i>P. t. troglodytes</i>, red - <i>P. t. ellioti</i>, blue - <i>P. t. verus</i>, green - <i>P. t. schweinfurthii</i>) with major rivers indicated. The Sanaga River in Cameroon has been proposed to form the boundary between the ranges of <i>P. t. ellioti</i> and <i>P. t. troglodytes</i>.</p

Pairwise F_ST values for human samples.

<p>Parentheses show the empirical central 95% region of the distribution of values for the 100 re-samples of the human data.</p

Structure estimates of ancestry in three populations.

<p>For each sampled individual the figure shows the estimated proportion of ancestry from Structure's three putative ancestral populations, with <i>P. t. troglodytes</i> in yellow, <i>P. t. ellioti</i> in red and <i>P. t. verus</i> in blue. Structure reveals the same pattern of group memberships as PCA, and additionally suggests that <i>P. t. troglodytes</i> and <i>P. t. ellioti</i> individuals may share more DNA from the other group than either shares with <i>P. t. verus</i> (blue). The two known hybrid individuals (C024, C025, with ancestry estimated at close to 50% in each of <i>P. t. troglodytes</i> and <i>P. t. verus</i>) and two <i>P. t. ellioti</i> chimpanzees with <i>P. t. troglodytes</i>-like mtDNA (C127, C541) are labelled.</p

Sequence data for exons 3 and 5 of the X-linked opsin gene (Indriidae)

Sequence alignments for exons 3 and 5 of the X-linked opsin gene. Data include consensus sequences for ten species of Indriidae. Alignments were generated in Geneious. The three key functional sites (180: exon 3, 277 and 285: exon 5) are highlighted (added in Adobe Illustrator)

Data from: Novel opsin gene variation in large-bodied, diurnal lemurs

Some primate populations include both trichromatic and dichromatic (red–green colour blind) individuals due to allelic variation at the X-linked opsin locus. This polymorphic trichromacy is well described in day-active New World monkeys. Less is known about colour vision in Malagasy lemurs, but, unlike New World monkeys, only some day-active lemurs are polymorphic, while others are dichromatic. The evolutionary pressures underlying these differences in lemurs are unknown, but aspects of species ecology, including variation in activity pattern, are hypothesized to play a role. Limited data on X-linked opsin variation in lemurs make such hypotheses difficult to evaluate. We provide the first detailed examination of X-linked opsin variation across a lemur clade (Indriidae). We sequenced the X-linked opsin in the most strictly diurnal and largest extant lemur, Indri indri, and nine species of smaller, generally diurnal indriids (Propithecus). Although nocturnal Avahi (sister taxon to Propithecus) lacks a polymorphism, at least eight species of diurnal indriids have two or more X-linked opsin alleles. Four rainforest-living taxa—I. indri and the three largest Propithecus species—have alleles not previously documented in lemurs. Moreover, we identified at least three opsin alleles in Indri with peak spectral sensitivities similar to some New World monkeys

Nucleotide alignment for exon 3 of the X-linked opsin gene (Indriidae)

Nucleotide alignment of consensus sequences for exon 3 of the X-linked opsin gene (Plain Text file in FASTA format generated in Geneious). Sequences represent 10 species of Indriidae