Uncovering adaptive evolution in the human lineage

Background

The recent increase in human polymorphism data, together with the availability of genome sequences from several primate species, provides an unprecedented opportunity to investigate how natural selection has shaped human evolution.

Results

We compared human branch-specific substitutions with variation data in the current human population to measure the impact of adaptive evolution on human protein coding genes. The use of single nucleotide polymorphisms (SNPs) with high derived allele frequencies (DAFs) minimized the influence of segregating slightly deleterious mutations and improved the estimation of the number of adaptive sites. Using DAF ≥ 60% we showed that the proportion of adaptive substitutions is 0.2% in the complete gene set. However, the percentage rose to 40% when we focused on genes that are specifically accelerated in the human branch with respect to the chimpanzee branch, or on genes that show signatures of adaptive selection at the codon level by the maximum likelihood based branch-site test. In general, neural genes are enriched in positive selection signatures. Genes with multiple lines of evidence of positive selection include taxilin beta, which is involved in motor nerve regeneration and syntabulin, and is required for the formation of new presynaptic boutons.

Conclusions

We combined several methods to detect adaptive evolution in human coding sequences at a genome-wide level. The use of variation data, in addition to sequence divergence information, uncovered previously undetected positive selection signatures in neural genes.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-599) contains supplementary material, which is available to authorized users.     

The evolution of an alpha-esterase pseudogene inactivated in the Drosophila melanogaster lineage

Previous analyses of the alpha-esterase cluster of Drosophila melanogaster revealed 10 active genes and the DmalphaE4a-Psi pseudogene. Here, we reconstruct the evolution of the pseudogene from the sequences of 12 alleles from widely scattered D. melanogaster populations and single alleles from Drosophila simulans and Drosophila yakuba. All of the DmalphaE4a-Psi alleles contain numerous inactivating mutations, suggesting that pseudogene alleles are fixed in natural populations. Several lines of evidence also suggest that DmalphaE4a is now evolving without selective constraint in the D. melanogaster lineage. There are three polymorphic indels which result in frameshifts; a key nucleotide of the intron splice acceptor is polymorphic; the neutral mutation parameter is the same for replacement and silent sites; one of the nonsilent polymorphisms results in a stop codon; only 1 of the 13 replacement polymorphisms is biochemically conservative; residues that are conserved among active esterases have different states in DmalphaE4a-Psi; and there are about half as many transitional polymorphisms as transversional ones. In contrast, the D. simulans and D. yakuba orthologs DsalphaE4a and DyalphaE4a do not have the inactivating mutations of DmalphaE4a-Psi and appear to be evolving under the purifying selection typical of protein- encoding genes. For instance, there have been more substitutions in the introns than in the exons, and more in silent sites than in replacement sites. Furthermore, most of the amino acid substitutions that have occurred between DyalphaE4a and DsalphaE4a are located in sites that typically vary among active alpha-esterases rather than those that are usually conserved. We argue that the original alphaE4a gene had a function which it has lost since the divergence of the D. melanogaster and D. simulans lineages.     

Acceleration of X-chromosome gene order evolution in the cattle lineage

The gene order on the X chromosome of eutherians is generally highly conserved, although an increase in the rate of rearrangement has been reported in the rodent lineage. Conservation of the X chromosome is thought to be caused by selection related to maintenance of dosage compensation. However, we herein reveal that the cattle (Btau4.0) lineage has experienced a strong increase in the rate of X-chromosome rearrangement, much stronger than that previously reported for rodents. We also show that this increase is not matched by a similar increase on the autosomes and cannot be explained by assembly errors. Furthermore, we compared the difference in two cattle genome assemblies: Btau4.0 and Btau6.0 (Bos taurus UMD3.1). The results showed a discrepancy between Btau4.0 and Btau6.0 cattle assembly version data, and we believe that Btau6.0 cattle assembly version data are not more reliable than Btau4.0. [BMB Reports 2013; 46(6): 310-315]     

Biomechanical consequences of rapid evolution in the polar bear lineage

The polar bear is the only living ursid with a fully carnivorous diet. Despite a number of well-documented craniodental adaptations for a diet of seal flesh and blubber, molecular and paleontological data indicate that this morphologically distinct species evolved less than a million years ago from the omnivorous brown bear. To better understand the evolution of this dietary specialization, we used phylogenetic tests to estimate the rate of morphological specialization in polar bears. We then used finite element analysis (FEA) to compare the limits of feeding performance in the polar bear skull to that of the phylogenetically and geographically close brown bear. Results indicate that extremely rapid evolution of semi-aquatic adaptations and dietary specialization in the polar bear lineage produced a cranial morphology that is weaker than that of brown bears and less suited to processing tough omnivorous or herbivorous diets. Our results suggest that continuation of current climate trends could affect polar bears by not only eliminating their primary food source, but also through competition with northward advancing, generalized brown populations for resources that they are ill-equipped to utilize.     

Punctuated stasis and collateral evolution in the Devonian lineage of Monograptus hercynicus

The changes in the sicula of Early Devonian monograptid graptolite populations show a pattern that is described as punctuated stasis: two longer periods of stasis separated by a transitional population of shorter duration between them. The pattern differs from punctuated equilibrium in that anagenesis is involved rather than cladogenesis. The pattern has been observed in several widely separated areas (Nevada, Thuringia, Poland, Ural Mountains) and is an example of collateral evolution in graptolites. In this case, the collateral morphologic change occurs relatively rapidly in a large, globally distributed taxon. The study permits accurate correlation of the horizon of appearance of Monograptus hercynicus Pemer in the upper delta Zone (conodont zonation) of late Lochkovian age (Devonian) on a global scale. The partial integration of these two biostratigraphies constrains correlations between the shelly, shallow-water biofacies and the deeper graptolitic biofacies. The pattern of punctuated stasis has been discovered in Lower Devonian strata of central Nevada, where 22 horizons in sequence were sampled. Statistical analyses were performed on 13 characters encompassing measurements of the sicula, thecae, and rhabdosome. Most of these characters do not exhibit sustained trends or punctuated changes. However, sicular width exhibits an abrupt increase over a short stratigraphic interval and is used to classify members of the group into four quantitatively defined morphotypes. This natural perturbation in the pattern of change is used to divide the lineage into paleospecies. This makes the segments of the lineage easy to identify and imparts stability to the classification and precision in biostratigraphy. The variation studies enable the ranges of the morphotypes to be used to further subdivide the stratigraphic record of the late Lochkovian. □ Graptolites, Devonian, Lochkovian, evolution, punctuated stasis, biostratigraphy, MONOGRAPTUS, phylogeny.     

The chicken IL-1 family: evolution in the context of the studied vertebrate lineage

The interleukin-1 gene family encodes a group of related proteins that exhibit a remarkable pleiotropy in the context of health and disease. The set of indispensable functions they control suggests that these genes should be found in all eukaryotic species. The ligands and receptors of this family have been primarily characterised in man and mouse. The genomes of most non-mammalian animal species sequenced so far possess all of the IL-1 receptor genes found in mammals. Yet, strikingly, very few of the ligands are identifiable in non-mammalian genomes. Our recent identification of two further IL-1 ligands in the chicken warranted a critical reappraisal of the evolution of this vitally important cytokine family. This review presents substantial data gathered across multiple, divergent metazoan genomes to unambiguously trace the origin of these genes. With the hypothesis that all of these genes, both ligands and receptors, were formed in a single ancient ancestor, extensive database mining revealed sufficient evidence to confirm this. It therefore suggests that the emergence of mammals is unrelated to the expansion of the IL-1 family. A thorough review of this cytokine family in the chicken, the most extensively studied amongst non-mammalian species, is also presented.     

Evidence for the evolution of tenascin and fibronectin early in the chordate lineage

Fibronectin and tenascin are extracellular matrix glycoproteins that play important roles in cell adhesion and motility. In a previous study we provided evidence that tenascin first appeared early in the chordate lineage. As tenascin has been proposed to act, in part, through modulation of cell-fibronectin interactions, we sought here to identify fibronectin genes in non-vertebrate chordates and other invertebrates to determine if tenascin and fibronectin evolved separately or together, and to identify phylogenetically conserved features of both proteins. We found that the genome of the urochordate Ciona savignyi contains both a tenascin gene and a gene encoding a fibronectin-like protein with fibronectin type 1, 2 and 3 repeats. The genome of the cephalochordate Branchiostoma floridae (amphioxus) also has a tenascin gene. However, we could not identify a fibronectin-like gene in B. floridae, nor could we identify fibronectin or tenascin genes in echinoderms, protostomes or cnidarians. If urochordates are more closely related to vertebrates, tenascin may have evolved before fibronectin in an ancestor common to tunicates and amphioxus. Alternatively, tenascin and fibronectin may have evolved in an ancestor common to B. floridae and C. savignyi and the fibronectin gene was subsequently lost in the cephalochordate lineage. The fibronectin-like gene from C. savignyi does not encode the RGD motif for integrin binding found in all vertebrate fibronectins, and it lacks most of the fibronectin type 1 domains believed to be critical for fibrillogenesis. In contrast, the tenascin gene in B. floridae encodes multiple RGD motifs, suggesting that integrin binding is fundamental to tenascin function.     

Gradual evolution in the African hunting dog lineage Systematic implications

The hunting dog, Lycaon pictus, is one of the most representative species of the extant African fauna and one of the most efficient predators in the World. This species is actually a relict within Sub-Saharan Africa, but its lineage is well recorded in Eurasia during the Pliocene, and in Eurasia and Africa during the Early Pleistocene, while its record during the Middle Pleistocene is not well documented. Though postcranial skeletal remains dating from the Early Pleistocene show a tetradactyl forelimb, a characteristic feature of the extant lycaon, unique among canids, the upper and lower dentitions show gradual evolution from a primitive morphology in the Late Pliocene specimens to the highly specialized trenchant carnassials of the extant predatory species. We propose a new systematics for the lineage, grouping all the forms within the genus Lycaon. To cite this article: B. Martínez-Navarro, L. Rook, C. R. Palevol 2 (2003).     

Regional integration of evidence for evolution in the Silurian Pentamerus-Pentameroides lineage

Under ideal conditions, the stratophenetic test for phyletic gradualism in fossil lineages requires nearly continuous samples of time-specific populations through rock sequences representing geologically significant periods of time. Shifting environments account for one source of 'imperfection' in the local rock record. Few species are sufficiently eurytopic to survive changing environments in a given region over a long time span. Where marine fossils are involved, independently correlated sea-level curves may be used to patch together segments of stratigraphic sections from different regions that collectively encompass the uninterrupted environment of the target species. In the Lower Silurian of Iowa, stratigraphic gaps among test samples for phyletic gradualism in pentamerid brachiopods occur wherever pentamerid communities are succeeded by deeper water stricklandiid communities or by shallower-water coral-algal communities. Correlation of sea-level curves indicates that water depth was consistently shallower in the northern Great Lakes area. Usually when stricklandiid communities replaced a pentamerid community in Iowan seas, contemporaneous pentamerid communities replaced a coral-algal community in Michigan or Ontario seas. Temporal meshing of samples from Iowa and the northern Great Lakes area (based on congruent Stricklandia and Eocoelia lineage zones) supports the hypothesis that Pentamerus oblongus evolved to Pentameroides subrectus through a gradual narrowing and loss of divergence in its outer plates. A transitional morphotype between the two genera (from the Lower Silurian of Alabama) is illustrated. □ Phyletic gradualism, punctuated equilibria, Brachiopoda, Pentamerida, Silurian, North America.     

Hominid evolution and the concept of techno-cultural dynamism in Africa

Archaeology treats hominid evlution as a bio-cultural phenomenon and reveals the behavioral activities of man as far back as 3 to 5 millions years ago, with different genera and species of hominids and their cultural endowment. Hominid evolution is also considered as exhibiting some technocultural dynamism. The relevance of this concept in the struggle for survival is focused upon in this paper. The ability of the hominids to explore and exploit the environment formed the basis of their survival. The paper concoludes that Africa as the cradle of hominid evolution has however lagged behind in global techno- cultural development.     

Correlates and catalysts of hominin evolution in Africa

Hominin evolution in the African Pliocene and Pleistocene was accompanied and mediated by changes in the abiotic and biotic spheres. It has been hypothesized that such environmental changes were catalysts of hominin morphological evolution and speciations. Whereas there is little doubt that ecological changes were relevant to shaping the trajectories of mammalian evolution, testing specific hypotheses with data from the fossil record has yielded ambiguous results regarding environmental disruption as a primary catalyst. Proposed mechanisms for abiotic and biotic causes of evolution are not always consistent with the timing and trends exhibited by the African fossil record of hominins and other mammals. Analyses of fossil and genetic data suggest that much of hominin evolution, and by extension mammalian evolution, was autocatalytic, driven by feedback loops within a species or lineage, irrespective of changes in the external environment.     

The biocultural evolution of Khoisan populations of Southern Africa

The research presented here offers new information on the recent evolution of Khoisan populations of southern Africa through the new study of Holocene skeletons. When combined with subfossil and historical remains, these archeological specimens provide a skeletal record for the last 5000–9000 years of southern African prehistory. Multivariate statistical analyses of cranial measurements were used to determine patterns of morphological variation in the skeletal record with which hypotheses of biocultural evolution were tested. These analyses yielded the following results. First, the traditional distinction between Bushmen and Hottentots holds for recent inland individuals. Second, there is a suggestion of a morphologically distinct San population living on the coast of South Africa. The idea of a “Strandloper” population suggested by early scholars is here revived. The third result is that there is little evidence of complete population succession on the coast of South Africa, suggesting that there were no massive population movements associated with the spread of Hottentot pastoralism throughout southern Africa.     

Out of Africa and the evolution of human behavior

Twenty‐one years ago, a landmark exploration of mitochondrial DNA diversity popularized the idea of a recent African origin for all living humans. 1 The ancestral African population was estimated to have existed 200 ka (thousands of years ago) plus or minus a few tens of thousands of years. A corollary was that at some later date the fully modern African descendants of that population expanded to swamp or replace the Neanderthals and other nonmodern Eurasians. The basic concept soon became known as “Out of Africa,” after the Academy Award winning film (1985) that took its title, in turn, from Isak Dinesen's classic autobiography (1937). Many subsequent genetic analyses, including those of Ingman and coworkers 2 and Underhill and coworkers, 3 have reaffirmed the fundamental Out of Africa model. The fossil and archeological records also support it strongly. The fossil record implies that anatomically modern or near‐modern humans were present in Africa by 150 ka; the fossil and archeological records together indicate that modern Africans expanded to Eurasia beginning about 50 ka.     

Hypervariable plastid locus variation and intron evolution in the Anacamptis palustris lineage.

Data on the organization of a hypervariable chloroplast locus in the Anacamptis palustris (Orchidaceae) lineage are provided and used to infer the pattern of molecular evolution in this group. A large survey of sequence variation in A. palustris and allied taxa reveals several repeat types differing in number and organization that occur in the same plastid region. The resulting repeat type network suggests that at least seven different minisatellite loci evolved near each other in the tRNALEU intron and indicates the presence of at least three main phyletic lines in the A. palustris lineage.     

Recent human evolution in northwestern Africa.

The first modern humans in the Maghreb are said to be associated with the Aterian industries which appeared at least 40 ka BP in the northwest. Their predecessors are mainly represented by the Jebel Irhoud (Morocco) specimens. Palaeontological evidence, as well as electron spin resonance (ESR) dating, suggests that this series is older than previously published, and should belong to oxygen isotope stage 5 or even 6. There is no evidence of any Neanderthal apomorphy in this group which can no longer be considered as 'African Nanderthals'. Clear synapomorphies with modern man combined with some plesiomorphic retentions indicate a slightly more primitive (and older?) grade than the Qafzeh-Skhul sample in southwestern Asia. The Northwestern evidence demonstrates that the mediterranean sea was a major biological barrier during the upper Middle and lower Upper Pleistocene and that the rise of anatomically modern features cannot be restricted to a sub-Saharan of eastern African area.     

Hominid evolution in Northwest Africa and the question of the North African Neanderthaloids

The North African evidence bearing on hominid evolution is summarized and reviewed in relation to its industrial associations and apparent chronological order. Three tacit suppositions of the past and their effects on taxonomy and thinking in evolutionary anthropology are examined, namely the concepts of a single and unique origin of Man, of the inherent and essential, distinction between physical and spiritual Man, and of physical resemblance as absolute proof of relationship. The consequent confusion and looseness of application which have characterized hominid taxonomy, especially concerning the term Neanderthal and its derivatives, are examined and discussed primarily in relation to the so-called Neanderthals of northern Africa. It is suggested that the Atlanthropus remains may represent not one but two hominid varieties. Further it is argued that none of the North African remains are demonstrably related to the European Neanderthals and that some at least of them seem clearly unrelated. In conclusion it is suggested that the hominid remains from Ternifine, the Littorina Cave (Casablanca), Témara, Rabat, Jebel Irhoud and Tangier may represent links in a North African chain of hominid evolution which developed locally and remained independent of all external influence during the period covered by those specimens.