Floral trait differentiation in Anacamptis coriophora: Phenotypic selection on scents,but not on colour

Current divergent selection may promote floral trait differentiation among conspecific populations in flowering plants. However, whether this applies to complex traits such as colour or scents has been little studied, even though these traits often vary within species. In this study, we compared floral colour and odour as well as selective pressures imposed upon these traits among seven populations belonging to three subspecies of the widespread, generalist orchid Anacamptis coriophora. Colour was characterized using calibrated photographs, and scents were sampled using dynamic headspace extraction and analysed using gas chromatography–mass spectrometry. We then quantified phenotypic selection exerted on these traits by regressing fruit set values on floral trait values. We showed that the three studied subspecies were characterized by different floral colour and odour, with one of the two predominant floral volatiles emitted by each subspecies being taxon‐specific. Plant size was positively correlated with fruit set in most populations, whereas we found no apparent link between floral colour and female reproductive success. We detected positive selection on several taxon‐specific compounds in A. coriophora subsp. fragrans, whereas no selection was found on floral volatiles of A. coriophora subsp. coriophora and A. coriophora subsp. martrinii. This study is one of the first to document variation in phenotypic selection exerted on floral scents among conspecific populations. Our results suggest that selection could contribute to ongoing chemical divergence among A. coriophora subspecies.     

Recent positive selection of a human androgen receptor/ectodysplasin A2 receptor haplotype and its relationship to male pattern baldness

Genetic variants in the human androgen receptor gene (AR) are associated with male pattern baldness (androgenetic alopecia, AGA) in Europeans. Previous observations of long-range linkage disequilibrium at the AR locus are consistent with the hypothesis of recent positive selection. Here, we further investigate this signature and its relationship to the AGA risk haplotype. The haplotype homozygosity suggests that the AGA risk haplotype was driven to high frequency by positive selection in Europeans although a low meiotic recombination rate contributed to the high haplotype homozygosity. Further, we find high levels of population differentiation as measured by F _ST and a series of fixed derived alleles along an extended region centromeric to AR in the Asian HapMap sample. The predominant AGA risk haplotype also carries the putatively functional variant 57K in the flanking ectodysplasin A2 receptor gene (EDA2R). It is therefore probable that the AGA risk haplotype rose to high frequency in combination with this EDA2R variant, possibly by hitchhiking on a positively selected 57K haplotype. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Positive selection underlies the species‐specific binding of Plasmodium falciparum RH5 to human basigin

Plasmodium falciparum, the causative agent of the deadliest form of malaria, is a member of the Laverania subgenus, which includes ape‐infecting parasites. P. falciparum is thought to have originated in gorillas, although infection is now restricted to humans. Laverania parasites display remarkable host‐specificity, which is partially mediated by the interaction between parasite ligands and host receptors. We analyse the evolution of BSG (basigin) and GYPA (glycophorin A) in primates/hominins, as well as of their Plasmodium‐encoded ligands, PfRH5 and PfEBA175. We show that, in primates, positive selection targeted two sites in BSG (F27 and H102), both involved in PfRH5 binding. A population genetics–phylogenetics approach detected the strongest selection for the gorilla lineage: one of the positively selected sites (K191) is a major determinant of PfRH5 binding affinity. Analysis of RH5 genes indicated episodic selection on the P. falciparum branch; the positively selected W447 site is known to stabilize the interaction with human basigin. Conversely, we detect no selection in the receptor‐binding region of EBA175 in the P. falciparum lineage. Its host receptor, GYPA, shows evidence of positive selection in all hominid lineages; selected codons include glycosylation sites that modulate PfEBA175 binding affinity. Data herein provide an evolutionary explanation for species‐specific binding of the PfRH5‐BSG ligand–receptor pair and support the hypothesis that positive selection at these genes drove the host shift leading to the emergence of P. falciparum as a human pathogen.     

News from the west: Ancient DNA from a French megalithic burial chamber

Recent paleogenetic studies have confirmed that the spread of the Neolithic across Europe was neither genetically nor geographically uniform. To extend existing knowledge of the mitochondrial European Neolithic gene pool, we examined six samples of human skeletal material from a French megalithic long mound (c.4200 cal BC). We retrieved HVR‐I sequences from three individuals and demonstrated that in the Neolithic period the mtDNA haplogroup N1a, previously only known in central Europe, was as widely distributed as western France. Alternative scenarios are discussed in seeking to explain this result, including Mesolithic ancestry, Neolithic demic diffusion, and long‐distance matrimonial exchanges. In light of the limited Neolithic ancient DNA (aDNA) data currently available, we observe that all three scenarios appear equally consistent with paleogenetic and archaeological data. In consequence, we advocate caution in interpreting aDNA in the context of the Neolithic transition in Europe. Nevertheless, our results strengthen conclusions demonstrating genetic discontinuity between modern and ancient Europeans whether through migration, demographic or selection processes, or social practices. Am J Phys Anthropol, 2010. © 2010 Wiley‐Liss, Inc.     

Brief communication: Population variation in human maxillary premolar accessory ridges (MxPAR)

The purpose of this brief communication is to report the results of an analysis of maxillary premolar accessory ridges (MxPAR), a common but understudied accessory ridge that may occur both mesial and distal to the central ridge of the buccal cusp of upper premolars. We developed a new five‐grade scoring plaque to better categorize MxPAR variation. Subsequently, we conducted a population analysis of MxPAR frequency in 749 dental casts of South African Indian, American Chinese, Alaskan Eskimo, Tohono O'odham (Papago), Akimel O'odham (Pima), Solomon Islander, South African Bantu, and both American and South African Whites. Northeast Asian and Asian‐derived populations exhibited the highest MxPAR frequencies while Indo‐European samples (South African Indians, American and South African Whites) exhibited relatively low frequencies. The Solomon Islanders and South African Bantu samples exhibited intermediate frequencies. Our analysis indicates that statistically significant differences in MxPAR frequency exist between major geographic populations. As a result, the MxPAR plaque has now been added to the Arizona State University Dental Anthropology System, an important contribution as maxillary premolar traits are underrepresented in analyses of dental morphology. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Pollinator‐mediated selection on floral size and tube color in Linum pubescens: Can differential behavior and preference in different times of the day maintain dimorphism?

Diversity of flower traits is often proposed as the outcome of selection exerted by pollinators. Positive directional pollinator‐mediated selection on floral size has been widely shown to reduce phenotypic variance. However, the underlying mechanism of maintaining within‐population floral color polymorphism is poorly understood. Divergent selection, mediated by different pollinators or by both mutualists and antagonists, may create and maintain such polymorphism, but it has rarely been shown to result from differential behavior of one pollinator. We tested whether different behaviors of the same pollinators in morning and evening are associated with dimorphic floral trait in Linum pubescens, a Mediterranean annual plant that exhibits variable within‐population frequencies of dark‐ and light‐colored flower tubes. Usia bicolor bee‐flies, the major pollinators of L. pubescens, are mostly feeding in the flower in the morning, while in the evening they are mostly visiting the flowers for mating. In 2 years of studying L. pubescens in a single large population in the Carmel, Israel, we found in one year that dark‐centered flowers received significantly higher fraction of visits in the morning. Fitness was positively affected by number of visits, but no fitness differences were found between tube‐color morphs, suggesting that both morphs have similar pollination success. Using mediation analysis, we found that flower size was under positive directional pollinator‐mediated selection in both years, but pollinator behavior did not explain entirely this selection, which was possibly mediated also by other agents, such as florivores or a‐biotic stresses. While most pollinator‐mediated selection studies show that flower size signals food reward, in L. pubescens, it may also signal for mating place, which may drive positive selection. While flower size found to be under pollinator‐mediated selection in L. pubescens, differential behavior of the pollinators in morning and evening did not seem to explain flower color polymorphism.     

Positive selection in MAOA gene is human exclusive: determination of the putative amino acid change selected in the human lineage

Monoamine oxidase A (MAOA) is the X-linked gene responsible for deamination and subsequent degradation of several neurotransmitters and other amines. Among other activities, the gene has been shown to play a role in locomotion, circadian rhythm, and pain sensitivity and to have a critical influence on behavior and cognition. Previous studies have reported a non-neutral evolution of the gene attributable to positive selection in the human lineage. To determine whether this selection was human-exclusive or shared with other species, we performed a population genetic analysis of the pattern of nucleotide variation in non-human species, including bonobo, chimpanzee, gorilla, and orangutan. Footprints of positive selection were absent in all analyzed species, suggesting that positive selection has been recent and unique to humans. To determine which human-unique genetic changes could have been responsible for this differential evolution, the coding region of the gene was compared between human, chimpanzee, and gorilla. Only one human exclusive non-conservative change is present in the gene: Glu151Lys. This human substitution affects protein dimerization according to a three-dimensional structural model that predicts a non-negligible functional shift. This is the only candidate position at present to have been selected to fixation in humans during an episode of positive selection. Divergence analysis among species has shown that, even under positive selection in the human lineage, the MAOA gene did not experience accelerated evolution in any of the analyzed lineages, and that tools such as K_a/K_s would not have detected the selective history of the gene.     

Links between the discovery of primates and anatomical comparisons with humans,the chain of being,our place in nature,and racism

I focus on the crucial links between the discovery of nonhuman primates by Westerners, discussions on our place in nature, the chain of being, racism, and the history of primate comparative anatomy and of so‐called “anatomical human racial studies.” Strikingly, for more than a millennium humans knew more about the internal anatomy of a single monkey species than about that of their own bodies. This is because Galen used monkeys to infer human anatomy, in line with the human‐animal continuity implied by the Greek notion of scala naturae. With the rise of Christianity, nonhuman primates were increasingly seen in a negative way. A more positive view emerged in the 14th century when nonhuman primates were directly studied/seen by Europeans, culminating in Tyson's 1699 work showing that chimps share more gross anatomical similarities with humans than with monkeys. However, the discomfort caused by this human‐chimp similarity then led to a new idea of animal‐human discontinuity, now related not to anatomy but to “civilization”: between Europeans vs. non‐Europeans + other primates. Moreover, Linnaeus' Systema Naturae and the emergence of “anatomical racial studies” influenced by Camper's craniology then led to even more extreme ideas, such as the notion that Europeans were both mentally and morphologically “ideal.” Unfortunately the biased and often incorrect “results” of such studies, combined with ideas based on Darwin's “struggle for survival”, became crucial in propaganda that lead to the rise of eugenics in the end of the 19th/first half of 20th centuries and that culminated in Nazism. Since the 1950s there has been an emphasis on the continuity/unity between all human groups and other primates, in great part influenced by what happened during World War 2. Reviews such as this one are, therefore, particularly necessary to illuminate and guard against attitudes against “the Other” and racist ideologies that are re‐emerging in modern political discourse across the globe.     

Body proportions of circumpolar peoples as evidenced from skeletal data: Ipiutak and Tigara (Point Hope) versus Kodiak Island Inuit

Given the well‐documented fact that human body proportions covary with climate (presumably due to the action of selection), one would expect that the Ipiutak and Tigara Inuit samples from Point Hope, Alaska, would be characterized by an extremely cold‐adapted body shape. Comparison of the Point Hope Inuit samples to a large (n > 900) sample of European and European‐derived, African and African‐derived, and Native American skeletons (including Koniag Inuit from Kodiak Island, Alaska) confirms that the Point Hope Inuit evince a cold‐adapted body form, but analyses also reveal some unexpected results. For example, one might suspect that the Point Hope samples would show a more cold‐adapted body form than the Koniag, given their more extreme environment, but this is not the case. Additionally, univariate analyses seldom show the Inuit samples to be more cold‐adapted in body shape than Europeans, and multivariate cluster analyses that include a myriad of body shape variables such as femoral head diameter, bi‐iliac breadth, and limb segment lengths fail to effectively separate the Inuit samples from Europeans. In fact, in terms of body shape, the European and the Inuit samples tend to be cold‐adapted and tend to be separated in multivariate space from the more tropically adapted Africans, especially those groups from south of the Sahara. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Increased positive selection pressure within the complementarity determining regions of the T‐cell receptor β gene in New World monkeys

Because of the long‐term co‐evolution of TCR and MHC molecules, numerous nucleotide substitutions have accumulated within the domains of TCRβ genes. We previously found that nonsynonymous nucleotide substitutions occurred more frequently in complementarity determining region (CDR)β than in CDRα, even though only a limited number of common marmoset (Callithrix jacchus) and human T‐cell receptor β variable (TRBV) sequences were compared. This interesting finding raised the question of whether the increased selective pressure within CDRβ was species‐specific. In this study, we identified 21 TRBV region sequences from the common marmoset and performed comparative sequence analyses of the T‐cell receptor α variable (TRAV) and TRBV regions from human, chimpanzee, rhesus monkey, cotton‐top tamarin, Ma's night monkey, and common marmoset. The ratios of the number of nonsynonymous nucleotide substitutions per site (d_N) to the d_S values (d_N/d_S) were less than 1 within the framework regions (FRs) of TRAV and TRBV region sequences, suggesting that purifying selection is largely dominant within the FRs. In contrast, the d_N values were statistically significantly greater for CDRβ than for CDRα only in New World monkeys. Also, increased d_N/d_S ratios (d_N/d_S>1) were observed within CDRβ between humans and New World monkeys and, interestingly, between New World monkeys, which share a relatively recent common ancestor. Moreover, phylogenetic analysis by maximum likelihood analysis provided firm evidence to support that positive selection occurred within CDRβ along New World monkey lineages. These results suggest that increased positive selection pressure within CDRβ is common in New World monkeys rather than being species‐specific. This study provides an intriguing insight into the co‐evolution of TCR and MHC molecules within primates. Am. J. Primatol. 73:1082–1092, 2011. © 2011 Wiley‐Liss, Inc.     

Fast and robust detection of ancestral selective sweeps

There are few methods tailored for detecting signals of positive selection in populations directly ancestral to multiple descendent populations. We introduce the ancestral branch statistic (ABS), a four‐population summary statistic for identifying selective sweeps occurring in the direct ancestor of a pair of populations. Simulations show that ABS performs at least as well as, and often better under model violations, than the complementary likelihood approach of 3P‐CLR across diverse selection scenarios and parameter values. We first applied ABS to contemporary human genomic data to identify genes that may have been adaptive in ancestral East Asian populations, uncovering the well‐established candidate EDAR, as well as a novel candidate SLC35F3, which encodes a putative thiamine transporter that may have been involved in adaptation to eating polished grains. Next, we performed scans with ancient European genomic data to reexamine evidence of recent positive selection in ancestral Europeans. The MCM6/LCT cluster and the SLC45A2 and HERC2 genes are strong outliers, agreeing with previous studies. Novel candidates, such as SLC30A9 and CYP1A2, may have been involved in adaptation to local nutrient sufficiency and lifestyle changes. Finally, we provide open‐source software, CalcABS, which can perform genomic scans of ancestral sweeps with ABS from population allele frequency data.     

The Hemimelic extra toes mouse mutant: Historical perspective on unraveling mechanisms of dysmorphogenesis

Hemimelic extra toes (Hx) arose spontaneously as a dominant mutation in B10.D2/nSnJ mice in 1967. It specifically affects the appendicular skeleton, causing variable foreshortening of the tibia (radius) and preaxial polydactylism. Early anatomical studies revealed anterior overgrowth of the autopod, with decreased apoptosis and increased mitosis in the anterior apical ectodermal ridge and underlying mesenchyme; overextension of apoptosis in the central zeugopod accounted for hemimelia. The Hx mutant phenotype was coarsely mapped to mouse chromosome (Chr) 5 and closely linked to engrailed‐2 (En2) and Sonic hedgehog (Shh). This region is syntenic to human Chr 7q36 that harbors several dominant mutations affecting the hand. High‐resolution genome mapping identified the Hx mutation as a G → A base pair transition within Intron 5 of the murine Lmbr1 locus. The critical effect is on a multifunctional conserved regulatory element that acts as a limb‐specific, long‐distance cis‐acting enhancer of Shh expression. As such, the Hx mutant phenotype results from ectopic Shh signals at the anterior margin of the limb bud that directly or indirectly alter FGF4 signaling from the apical ectodermal ridge. Given significant advances in understanding of embryonic development in general and limb development in particular, this review article reveals how research that once attracted interest of teratologists has advanced across the decades to pinpoint a critical molecular lesion and reveal a potential mechanism of a specific malformation that is found commonly in experimental teratology. Birth Defects Research (Part C) 90:155–162, 2010. © 2010 Wiley‐Liss, Inc.     

Identifying genes underlying skin pigmentation differences among human populations

Skin pigmentation is a human phenotype that varies greatly among human populations and it has long been speculated that this variation is adaptive. We therefore expect the genes that contribute to these large differences in phenotype to show large allele frequency differences among populations and to possibly harbor signatures of positive selection. To identify the loci that likely contribute to among-population human skin pigmentation differences, we measured allele frequency differentiation among Europeans, Chinese and Africans for 24 human pigmentation genes from 2 publicly available, large scale SNP data sets. Several skin pigmentation genes show unusually large allele frequency differences among these populations. To determine whether these allele frequency differences might be due to selection, we employed a within-population test based on long-range haplotype structure and identified several outliers that have not been previously identified as putatively adaptive. Most notably, we identify the DCT gene as a candidate for recent positive selection in the Chinese. Moreover, our analyses suggest that it is likely that different genes are responsible for the lighter skin pigmentation found in different non-African populations. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Genome‐wide detection of signatures of selection in Korean Hanwoo cattle

The Korean Hanwoo cattle have been intensively selected for production traits, especially high intramuscular fat content. It is believed that ancient crossings between different breeds contributed to forming the Hanwoo, but little is known about the genomic differences and similarities between other cattle breeds and the Hanwoo. In this work, cattle breeds were grouped by origin into four types and used for comparisons: the Europeans (represented by six breeds), zebu (Nelore), African taurine (N'Dama) and Hanwoo. All animals had genotypes for around 680 000 SNPs after quality control of genotypes. Average heterozygosity was lower in Nelore and N'Dama (0.22 and 0.21 respectively) than in Europeans (0.26–0.31, with Shorthorn as outlier at 0.24) and Hanwoo (0.29). Pairwise F_ST analyses demonstrated that Hanwoo are more related to European cattle than to Nelore, with N'Dama in an intermediate position. This finding was corroborated by principal components and unsupervised hierarchical clustering. Using genome‐wide smoothed F_ST, 55 genomic regions potentially under positive selection in Hanwoo were identified. Among these, 29 were regions also detected in previous studies. Twenty‐four regions were exclusive to Hanwoo, and a number of other regions were shared with one or two of the other groups. These regions overlap a number of genes that are related to immune, reproduction and fatty acid metabolism pathways. Further analyses are needed to better characterize the ancestry of the Hanwoo cattle and to define the genes responsible to the identified selection peaks.     

Evidence for recent positive selection at the human AIM1 locus in a European population

Two missense polymorphisms (E272K and L374F) of the AIM1 locus,encoding a melanocyte differentiation antigen, were shown tohave a clear association with human ethnicities. These two nonpathogenicsingle nucleotide polymorphisms (SNPs) may be associated withhuman pigmentation variation. In this study, we investigatedsequence variation in the coding region and exon-flanking sequenceand found low genetic variation only in subjects of Europeandescent. All four statistical tests applied to the 7.55-kb regionsurrounding the L374F polymorphism detected statistically significantdeviations from selective neutrality in Europeans. In addition,haplotype analysis revealed that one haplotype carrying 374Fwas overrepresented in this population, and the low rate ofvariation, with some features of selective sweeps, was shownto be statistically significant. These results suggest thatpositive selection recently has been acting or has acted onat least this region of the melanogenic gene and that an advantageoushaplotype spread rapidly in Europe.     

Williams-Beuren mapping in Callithrix argentata, Callicebus cupreus and Alouatta caraya indicates different patterns of chromosomal rearrangements in neotropical primates

Human chromosome 7 has a complex syntenic origin. It was divided into two segments in both the ancestral primate karyotype and in Platyrrhini. Apparently, a small segment in the ancestral platyrrhine karyotype was associated with HSA5 and the remainder formed a middle‐sized submetacentric. We tested the dynamics of platyrrhine chromosomes by hybridizing the locus specific Willams‐Beuren probe (7q 11.23, 450 kb) to chromosomes of representative species from the three families of the New World monkeys recently proposed by molecular genomics: Cebidae, Callithrix argentata (bare ear marmoset or silvery marmoset, 2n = 44); Pitheciidae, Callicebus cupreus [red titi monkey, or coppery monkey, 2n = 46)] and Atelidae, Alouatta caraya (black and gold howler, 2n = 52). In both the marmoset and the howler monkeys, the signal was found on the small segment of chromosome 7 associated with human chromosome 5, but not in Callicebus cupreus. Instead, the Williams‐Beuren syndrome (WS) signal was found on a C. cupreus chromosome previously reported to be hybridized only by human chromosome 1. The WS probe indicates a small, but complex translocation never described before. Our results point out that fluorescence in situ hybridization (FISH) with locus specific probes and cloned DNA fragments such as bacterial aftificial chromosomes (BACs) provides higher resolution than FISH with whole chromosomes paints. It may be well that the variability seen in the hybridization patterns and revealed by the WS FISH in this report is as a result of a rearrangement ‘hot spot’. The WS region in humans is composed of region‐specific different blocks of complex segmental duplications that probably promote the extraordinary rate of evolutionary dynamics of this region among primate species, and which continues to be reflected today by the predisposition of this region to disease syndromes such as WS. The evolutionary history of this region also suggests that repeat families in this region had their origin in a common ancestor of both Old World and New World monkeys.     

A haplotype method detects diverse scenarios of local adaptation from genomic sequence variation

Identifying genomic targets of population‐specific positive selection is a major goal in several areas of basic and applied biology. However, it is unclear how often such selection should act on new mutations versus standing genetic variation or recurrent mutation, and furthermore, favoured alleles may either become fixed or remain variable in the population. Very few population genetic statistics are sensitive to all of these modes of selection. Here, we introduce and evaluate the Comparative Haplotype Identity statistic (χ_MD), which assesses whether pairwise haplotype sharing at a locus in one population is unusually large compared with another population, relative to genomewide trends. Using simulations that emulate human and Drosophila genetic variation, we find that χ_MD is sensitive to a wide range of selection scenarios, and for some very challenging cases (e.g. partial soft sweeps), it outperforms other two‐population statistics. We also find that, as with F_ST, our haplotype approach has the ability to detect surprisingly ancient selective sweeps. Particularly for the scenarios resembling human variation, we find that χ_MD outperforms other frequency‐ and haplotype‐based statistics for soft and/or partial selective sweeps. Applying χ_MD and other between‐population statistics to published population genomic data from D. melanogaster, we find both shared and unique genes and functional categories identified by each statistic. The broad utility and computational simplicity of χ_MD will make it an especially valuable tool in the search for genes targeted by local adaptation.