Patterns of genetic variation and the role of selection in HTR1A and HTR1B in macaques (Macaca)

Research has increasingly highlighted the role of serotonin in behavior. However, few researchers have examined serotonin in an evolutionary context, although such research could provide insight into the evolution of important behaviors. The genus Macaca represents a useful model to address this, as this genus shows a wide range of behavioral variation. In addition, many genetic features of the macaque serotonin system are similar to those of humans, and as common models in biomedical research, knowledge of the genetic variation and evolution of serotonin functioning in macaques are particularly relevant for studies of human evolution. Here, we examine the role of selection in the macaque serotonin system by comparing patterns of genetic variation for two genes that code for two types of serotonin receptors – HTR1A and HTR1B – across five species of macaques. The pattern of variation is significantly different for HTR1A compared to HTR1B. Specifically, there is an increase in between-species variation compared to within-species variation for HTR1A. Phylogenetic analyses indicate that portions of HTR1A show an elevated level of nonsynonymous substitutions. Together these analyses are indicative of positive selection acting on HTR1A, but not HTR1B. Furthermore, the haplotype network for HTR1A is inconsistent with the species tree, potentially due to both deep coalescence and selection. The results of this study indicate distinct evolutionary histories for HTR1A and HTR1B, with HTR1A showing evidence of selection and a high level of divergence among species, a factor which may have an impact on biomedical research that uses these species as models. The wide genetic variation of HTR1A may also explain some of the species differences in behavior, although further studies on the phenotypic effect of the sequenced polymorphisms are needed to confirm this

The Molecular Evolution of the Serotonin System in Macaques (MACACA): a Detailed Survey of Four Serotonin-Related Genes

Serotonin, a hormone produced in the brain, has long been implicated in the regulation of critical behaviors, such as those related to aggression or impulse control. However, most research on serotonin has focused on the proximate connection to behavior, and little is known about its evolution. This is unfortunate, since the serotonin system has great potential to inform our understanding of behavioral evolution. I seek to address this gap in knowledge by investigating the molecular evolution of the serotonin system in macaques (genus Macaca). The macaque genus represents a useful model for understanding behavioral evolution. Comprised of approximately 19 species, macaques display a wide range of behaviors. It is likely that behavioral differences are caused by differences in neuroendocrinology. Therefore, the serotonin system provides one potential mechanism through which evolution may act to shape macaque behavior. In this dissertation, I sequence four genes that are known to influence serotonin functioning and behavior: HTR1A, HTR1B, TPH2, and SLC6A4. I examine the pattern of genetic variation within and between several species of macaque, and, using an approach based on molecular evolutionary theory, discern which evolutionary force ??? positive selection, balancing selection, purifying selection, or random genetic drift ??? is most likely to have acted on these genes. Three out of the four genes (HTR1B, TPH2, and SLC6A4), show a low level of overall genetic variation within the coding regions, suggesting that purifying selection is the predominate force acting on these genes. Within non-coding regions, the patterns of genetic variation found are consistent with genetic drift. Thus, positive selection does not seem to be affecting these genes. The genetic variation for these genes may contribute to the behavioral variation found in macaques; however, any effect that these genes have on behavior is likely due to non-adaptive evolutionary forces. In contrast to the other genes, HTR1A shows a pattern that is clearly distinct. HTR1A displays an unusually high level of interspecific variation, which is consistent with positive selection. Moreover, a subset of macaque species share a codon loss, an extremely rare event in gene evolution, and analyses of the coding region indicate a significant elevation of protein evolution among certain sites of the gene. These results suggest that positive selection has played a significant role in the evolution of the serotonin system and it is likely that the effects of positive selection on HTR1A contributed to macaque behavioral evolution. This research provides an important first step towards gaining a more thorough understanding of the mechanisms underlying the evolution of behavior

Data from: Encephalization and longevity evolved in a correlated fashion in Euarchontoglires but not in other mammals

Across mammals, encephalization and longevity show a strong correlation. It is not clear, however, whether these traits evolved in a correlated fashion within mammalian orders, or when they do, whether one trait drives changes in the other. Here, we compare independent and correlated evolutionary models to identify instances of correlated evolution within six mammalian orders. In cases of correlated evolution, we subsequently examined transition patterns between small/large relative brain size and short/long lifespan. In four mammalian orders, these traits evolved independently. This may reflect constraints related to energy allocation, predation avoidance tactics, and reproductive strategies. Within both primates and rodents, and their parent clade Euarchontoglires, we found evidence for correlated evolution. In primates, transition patterns suggest relatively larger brains likely facilitated the evolution of long lifespans. Because larger brains prolong development and reduce fertility rates, they may be compensated for with longer lifespans. Furthermore, encephalization may enable cognitively-complex strategies that reduce extrinsic mortality. Rodents show an inverse pattern of correlated evolution, whereby long lifespans appear to have facilitated the evolution of relatively larger brains. This may be because longer-lived organisms have more to gain from investment in encephalization. Together, our results provide evidence for the correlated evolution of encephalization and longevity, but only in some mammalian orders

Evolution_DeCasien et al_Supplementary Data

This excel file contains all data used in the manuscript "Encephalization and longevity evolved in a correlated fashion in Euarchontoglires but not in other mammals". Specifically, this data set contains maximum lifespans, species average brain weights, and species average body weights for more than 600 mammalian species, including 151 carnivorans (Carnivora), 77 even-toed ungulates (Artiodactyla), 37 cetaceans (Cetacea), and 54 chiropterans (Chiroptera) among Laurasiatheria, and 168 rodents (Rodentia), 10 lagomorphs (Lagomorpha), 3 tree shrews (Scandentia), and 144 primates (Primates) among Euarchontoglires

Evolutionary relationships of Macaca fascicularis fascicularis (Raffles 1821) (Primates: Cercopithecidae) from Singapore revealed by Bayesian analysis of mitochondrial DNA sequences

Schillaci, Michael A., Klegarth, Amy R., Switzer, William M., Shattuck, Milena R., Lee, Benjamin P. Y-H., Hollocher, Hope (2017): Evolutionary relationships of Macaca fascicularis fascicularis (Raffles 1821) (Primates: Cercopithecidae) from Singapore revealed by Bayesian analysis of mitochondrial DNA sequences. Raffles Bulletin of Zoology 65: 3-19, DOI: http://doi.org/10.5281/zenodo.535578

Patterns of Admixture and Population Structure in Native Populations of Northwest North America

The initial contact of European populations with indigenous populations of the Americas produced diverse admixture processes across North, Central, and South America. Recent studies have examined the genetic structure of indigenous populations of Latin America and the Caribbean and their admixed descendants, reporting on the genomic impact of the history of admixture with colonizing populations of European and African ancestry. However, relatively little genomic research has been conducted on admixture in indigenous North American populations. In this study, we analyze genomic data at 475,109 single-nucleotide polymorphisms sampled in indigenous peoples of the Pacific Northwest in British Columbia and Southeast Alaska, populations with a well-documented history of contact with European and Asian traders, fishermen, and contract laborers. We find that the indigenous populations of the Pacific Northwest have higher gene diversity than Latin American indigenous populations. Among the Pacific Northwest populations, interior groups provide more evidence for East Asian admixture, whereas coastal groups have higher levels of European admixture. In contrast with many Latin American indigenous populations, the variance of admixture is high in each of the Pacific Northwest indigenous populations, as expected for recent and ongoing admixture processes. The results reveal some similarities but notable differences between admixture patterns in the Pacific Northwest and those in Latin America, contributing to a more detailed understanding of the genomic consequences of European colonization events throughout the Americas

Procrustes-transformed multidimensional scaling plots of Eurasian and American individuals.

<p>(A) 641 individuals from 53 populations after resampling of 82 individuals from each of 14 nonoverlapping groups of European, Central and South Asian, East Asian, and American populations (<a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530.s007" target="_blank">Figure S7</a>). (B) 641 individuals from 41 populations after resampling of 82 individuals from each of 15 nonoverlapping groups of European, East Asian, and American populations (<a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530.s008" target="_blank">Figure S8</a>). (C) 393 individuals from 22 populations after resampling of 82 individuals from each of 10 nonoverlapping groups of European and American populations (<a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530.s009" target="_blank">Figure S9</a>). (D) 450 individuals from 34 populations after resampling of 82 individuals from each of 11 nonoverlapping groups of East Asian and American populations (<a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530.s010" target="_blank">Figure S10</a>). Procrustes similarity statistics are <i>t</i>₀ = 0.958 between <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g004" target="_blank">Figures 4B</a> and <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g005" target="_blank">5A</a>, <i>t</i>₀ = 0.999 between <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g005" target="_blank">Figures 5A and 5B</a>, <i>t</i>₀ = 0.956 between <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g005" target="_blank">Figures 5B and 5C</a>, and <i>t</i>₀ = 0.997 between <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g005" target="_blank">Figures 5B and 5D</a>. Population colors and symbols follow <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g001" target="_blank">Figure 1</a>.</p

Time of European and East-Asian admixture in North and Central America estimated using the admixture linkage disequilibrium approach in <i>ALDER</i>[44].

α<p>Populations considered as admixed populations using <i>ALDER</i><a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530-Loh1" target="_blank">[44]</a>.</p>β<p>Sets of European populations considered separately in <i>ALDER</i><a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530-Loh1" target="_blank">[44]</a> as reference populations for admixture.</p><p><i>EurA</i> : Toscani (TSI); Caucasian (CEU); Russian; Basque; French; Sardinian.</p><p><i>EurB</i> : Toscani (TSI); Basque ; French; Sardinian.</p><p><i>EurC</i> : Toscani (TSI); Caucasian (CEU); Basque; French; Sardinian.</p>γ<p><i>Sets of</i> East Asian populations considered separately in <i>ALDER</i><a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530-Loh1" target="_blank">[44]</a> as reference populations for admixture.</p><p><i>na</i>: No significant admixture was found with any of the reference populations considered.</p><p><i>AsA</i> : Japanese (JPT); Japanese.</p><p><i>AsB</i> : Han; Han (CHB); Han (CHD); Japanese (JPT); Japanese.</p><p><i>AsC</i> : Han; Han (CHB); Han (CHD); Japanese (JPT); Japanese; Yakut.</p>δ<p>Mean admixture time in years (25 years for generation time) estimated by <i>ALDER</i><a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530-Loh1" target="_blank">[44]</a> across the reference populations considered ± mean of the admixture time standard deviations obtained across the reference populations considered.</p>∈<p>Mean admixture rate estimated by <i>ALDER </i><a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530-Loh1" target="_blank">[<i>44</i>]</a> across the reference populations considered ± standard deviation.</p

Worldwide Admixture structure.

<p>Plotted are modes with clustering solutions obtained with 30 replicates at each value of <i>K</i>. Values of <i>K</i> and the number of runs in the mode shown appear on the left. In each plot, each cluster is represented by a different color, and each individual is represented by a vertical line divided into <i>K</i> colored segments with heights proportional to genotype memberships in the clusters. Thin black lines separate individuals from different populations. The same 528 individuals included in <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g004" target="_blank">Figure 4B</a> are considered in the Admixture analyses. Alternate clustering solutions for values of <i>K</i> from 2 to 12 appear in <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530.s003" target="_blank">Figure S3</a>.</p

Individual-level population structure.

<p>(A) Multidimensional scaling plot of pairwise allele-sharing distance (ASD) among 2,140 individuals in the combined dataset. (B) Multidimensional scaling plot of pairwise ASD among 528 individuals from 63 worldwide populations, following the resampling of a maximum of 82 individuals each from 11 different population groups. Group choices for resampling were taken from <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530.s006" target="_blank">Figure S6</a>. Population colors and symbols follow <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g001" target="_blank">Figure 1</a>.</p