Primate Family Research Articles

Patterns of dental emergence in early anthropoid primates from the Fayum Depression, Egypt

Paleontological field work in the Fayum Depression of Egypt has produced a remarkable diversity of fossil anthropoids, and this, combined with advances in genetic analyses of living anthropoids, has led to establishment of a temporal and phylogenetic framework for anthropoids that is achieving some degree of consensus. Less well understood are the evolutionary mechanisms and selective factors behind the origin and early diversification of anthropoids. One area that has remained under explored is investigation into the life history patterns of early anthropoids, a major omission given that understanding patterns of growth and development is essential for interpreting the paleobiology of fossil species. Here we detail dental emergence sequences for five species in four families of early anthropoid primates from the Fayum, and use these data to test Schultz’s Rule concerning the timing of emergence of molars versus premolars in mammals. Two important results are generated: (1) only one species had a dental eruption sequence identical to that observed among crown catarrhine primates; and (2) in all cases, the permanent canine was the last post-incisor dental element to fully erupt, a finding that may be significant for interpreting early anthropoid behavioral strategies.

Diversity starts early: notharctid primates from the Sandcouleean (Early Eocene) of the Powder River Basin, Wyoming, USA

Abundant specimens, mostly isolated teeth, of the Primate family Notharctidae occur in the Early Eocene rocks of the Powder River Basin of northeastern Wyoming, USA. Very early in the North American history of the family, the notharctid species diversified and this diversity may have been widespread, and not restricted to more southerly areas in the Rocky Mountains. The diversity is shown by detailed analysis of the molar dentition. Two new genera are established: Megaceralemur with Megaceralemur trigonodus as its type and Megaceralemur matthewi sp. nov. as a Sandcouleean species and Pinolophus, with Pinolophus meikei sp. nov. as its type, for a form with an entoconid notch on lower molar 1. Megaceralemur has a prominent nannopithex-fold which dominates the posterior cingulum of upper molars 1–2 and a cristid obliqua on lower molar 1 which attaches to the metaconid, not the metalophid as it does in Cantius and other genera. A small species, Cantius lohseorum sp. nov., is named for a derived lineage the size of Cantius torresi.urn:lsid:zoobank.org:pub:066DC515-A2DD-40AF-AD8A-3834E2AFD0FB

Multicopy gene family evolution on primate Y chromosomes.

BackgroundThe primate Y chromosome is distinguished by a lack of inter-chromosomal recombination along most of its length, extensive gene loss, and a prevalence of repetitive elements. A group of genes on the male-specific portion of the Y chromosome known as the “ampliconic genes” are present in multiple copies that are sometimes part of palindromes, and that undergo a form of intra-chromosomal recombination called gene conversion, wherein the nucleotides of one copy are homogenized by those of another. With the aim of further understanding gene family evolution of these genes, we collected nucleotide sequence and gene copy number information for several species of papionin monkey. We then tested for evidence of gene conversion, and developed a novel statistical framework to evaluate alternative models of gene family evolution using our data combined with other information from a human, a chimpanzee, and a rhesus macaque.ResultsOur results (i) recovered evidence for several novel examples of gene conversion in papionin monkeys and indicate that (ii) ampliconic gene families evolve faster than autosomal gene families and than single-copy genes on the Y chromosome and that (iii) Y-linked singleton and autosomal gene families evolved faster in humans and chimps than they do in the other Old World Monkey lineages we studied.ConclusionsRapid evolution of ampliconic genes cannot be attributed solely to residence on the Y chromosome, nor to variation between primate lineages in the rate of gene family evolution. Instead other factors, such as natural selection and gene conversion, appear to play a role in driving temporal and genomic evolutionary heterogeneity in primate gene families.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-2187-8) contains supplementary material, which is available to authorized users.

A collection of non-human primate computed tomography scans housed in MorphoSource, a repository for 3D data

A dataset of high-resolution microCT scans of primate skulls (crania and mandibles) and certain postcranial elements was collected to address questions about primate skull morphology. The sample consists of 489 scans taken from 431 specimens, representing 59 species of most Primate families. These data have transformative reuse potential as such datasets are necessary for conducting high power research into primate evolution, but require significant time and funding to collect. Similar datasets were previously only available to select research groups across the world. The physical specimens are vouchered at Harvard’s Museum of Comparative Zoology. The data collection took place at the Center for Nanoscale Systems at Harvard. The dataset is archived on MorphoSource.org. Though this is the largest high fidelity comparative dataset yet available, its provisioning on a web archive that allows unlimited researcher contributions promises a future with vastly increased digital collections available at researchers’ finger tips.

Molecular Evolution of the Glycosyltransferase 6 Gene Family in Primates.

Glycosyltransferase 6 gene family includes ABO, Ggta1, iGb3S, and GBGT1 genes and by three putative genes restricted to mammals, GT6m6, GTm6, and GT6m7, only the latter is found in primates. GT6 genes may encode functional and nonfunctional proteins. Ggta1 and GBGT1 genes, for instance, are pseudogenes in catarrhine primates, while iGb3S gene is only inactive in human, bonobo, and chimpanzee. Even inactivated, these genes tend to be conversed in primates. As some of the GT6 genes are related to the susceptibility or resistance to parasites, we investigated (i) the selective pressure on the GT6 paralogs genes in primates; (ii) the basis of the conservation of iGb3S in human, chimpanzee, and bonobo; and (iii) the functional potential of the GBGT1 and GT6m7 in catarrhines. We observed that the purifying selection is prevalent and these genes have a low diversity, though ABO and Ggta1 genes have some sites under positive selection. GT6m7, a putative gene associated with aggressive periodontitis, may have regulatory function, but experimental studies are needed to assess its function. The evolutionary conservation of iGb3S in humans, chimpanzee, and bonobo seems to be the result of proximity to genes with important biological functions.

The evolution of gene expression and binding specificity of the largest transcription factor family in primates.

The KRAB-containing zinc finger (KRAB-ZF) proteins represent the largest family of transcription factors (TFs) in humans, yet for the great majority, their function and specific genomic target remain unknown. However, it has been shown that a large fraction of these genes arose from segmental duplications, and that they have expanded in gene and zinc finger number throughout vertebrate evolution. To determine whether this expansion is linked to selective pressures acting on different domains, we have manually curated all KRAB-ZF genes present in the human genome together with their orthologous genes in three closely related species and assessed the evolutionary forces acting at the sequence level as well as on their expression profiles. We provide evidence that KRAB-ZFs can be separated into two categories according to the polymorphism present in their DNA-contacting residues. Those carrying a nonsynonymous single nucleotide polymorphism (SNP) in their DNA-contacting amino acids exhibit significantly reduced expression in all tissues, have emerged in a recent lineage, and seem to be less strongly constrained evolutionarily than those without such a polymorphism. This work provides evidence for a link between age of the TF, as well as polymorphism in their DNA-contacting residues and expression levels-both of which may be jointly affected by selection.

Molecular evolution and expression profile of the chemerine encoding gene RARRES2 in baboon and chimpanzee.

BackgroundChemerin, encoded by the retinoic acid receptor responder 2 (RARRES2) gene is an adipocytesecreted protein with autocrine/paracrine functions in adipose tissue, metabolism and inflammation with a recently described function in vascular tone regulation, liver, steatosis, etc. This molecule is believed to represent a critical endocrine signal linking obesity to diabetes. There are no data available regarding evolution of RARRES2 in non-human primates and great apes. Expression profile and orthology in RARRES2 genes are unknown aspects in the biology of this multigene family in primates. Thus; we attempt to describe expression profile and phylogenetic relationship as complementary knowledge in the function of this gene in primates. To do that, we performed A RT-PCR from different tissues obtained during necropsies. Also we tested the hypotheses of positive evolution, purifying selection, and neutrality. And finally a phylogenetic analysis was made between primates RARRES2 protein.ResultsRARRES2 transcripts were present in liver, lung, adipose tissue, ovary, pancreas, heart, hypothalamus and pituitary tissues. Expression in kidney and leukocytes were not detectable in either species. It was determined that the studied genes are orthologous.ConclusionsRARRES2 evolution fits the hypothesis of purifying selection. Expression profiles of the RARRES2 gene are similar in baboons and chimpanzees and are also phylogenetically related.

Overlapping Patterns of Rapid Evolution in the Nucleic Acid Sensors cGAS and OAS1 Suggest a Common Mechanism of Pathogen Antagonism and Escape.

A diverse subset of pattern recognition receptors (PRRs) detects pathogen-associated nucleic acids to initiate crucial innate immune responses in host organisms. Reflecting their importance for host defense, pathogens encode various countermeasures to evade or inhibit these immune effectors. PRRs directly engaged by pathogen inhibitors often evolve under recurrent bouts of positive selection that have been described as molecular ‘arms races.’ Cyclic GMP-AMP synthase (cGAS) was recently identified as a key PRR. Upon binding cytoplasmic double-stranded DNA (dsDNA) from various viruses, cGAS generates the small nucleotide secondary messenger cGAMP to signal activation of innate defenses. Here we report an evolutionary history of cGAS with recurrent positive selection in the primate lineage. Recent studies indicate a high degree of structural similarity between cGAS and 2’-5’-oligoadenylate synthase 1 (OAS1), a PRR that detects double-stranded RNA (dsRNA), despite low sequence identity between the respective genes. We present comprehensive comparative evolutionary analysis of cGAS and OAS1 primate sequences and observe positive selection at nucleic acid binding interfaces and distributed throughout both genes. Our data revealed homologous regions with strong signatures of positive selection, suggesting common mechanisms employed by unknown pathogen encoded inhibitors and similar modes of evasion from antagonism. Our analysis of cGAS diversification also identified alternately spliced forms missing multiple sites under positive selection. Further analysis of selection on the OAS family in primates, which comprises OAS1, OAS2, OAS3 and OASL, suggests a hypothesis where gene duplications and domain fusion events result in paralogs that provide another means of escaping pathogen inhibitors. Together our comparative evolutionary analysis of cGAS and OAS provides new insights into distinct mechanisms by which key molecular sentinels of the innate immune system have adapted to circumvent viral-encoded inhibitors.

An MRPS12 mutation modifies aminoglycoside sensitivity caused by 12S rRNA mutations.

Several homoplasmic pathologic mutations in mitochondrial DNA, such as those causing Leber hereditary optic neuropathy or non-syndromic hearing loss, show incomplete penetrance. Therefore, other elements must modify their pathogenicity. Discovery of these modifying factors is not an easy task because in multifactorial diseases conventional genetic approaches may not always be informative. Here, we have taken an evolutionary approach to unmask putative modifying factors for a particular homoplasmic pathologic mutation causing aminoglycoside-induced and non-syndromic hearing loss, the m.1494C>T transition in the mitochondrial DNA. The mutation is located in the decoding site of the mitochondrial ribosomal RNA. We first looked at mammalian species that had fixed the human pathologic mutation. These mutations are called compensated pathogenic deviations because an organism carrying one must also have another that suppresses the deleterious effect of the first. We found that species from the primate family Cercopithecidae (old world monkeys) harbor the m.1494T allele even if their auditory function is normal. In humans the m.1494T allele increases the susceptibility to aminoglycosides. However, in primary fibroblasts from a Cercopithecidae species, aminoglycosides do not impair cell growth, respiratory complex IV activity and quantity or the mitochondrial protein synthesis. Interestingly, this species also carries a fixed mutation in the mitochondrial ribosomal protein S12. We show that the expression of this variant in a human m.1494T cell line reduces its susceptibility to aminoglycosides. Because several mutations in this human protein have been described, they may possibly explain the absence of pathologic phenotype in some pedigree members with the most frequent pathologic mutations in mitochondrial ribosomal RNA.

Eco-evo-devo of the lemur syndrome: did adaptive behavioral plasticity get canalized in a large primate radiation?

BackgroundComprehensive explanations of behavioral adaptations rarely invoke all levels famously admonished by Niko Tinbergen. The role of developmental processes and plasticity, in particular, has often been neglected. In this paper, we combine ecological, physiological and developmental perspectives in developing a hypothesis to account for the evolution of ‘the lemur syndrome’, a combination of reduced sexual dimorphism, even adult sex ratios, female dominance and mild genital masculinization characterizing group-living species in two families of Malagasy primates.ResultsWe review the different components of the lemur syndrome and compare it with similar adaptations reported for other mammals. We find support for the assertion that the lemur syndrome represents a unique set of integrated behavioral, demographic and morphological traits. We combine existing hypotheses about underlying adaptive function and proximate causation by adding a potential developmental mechanism linking maternal stress and filial masculinization, and outline an evolutionary scenario for its canalization.ConclusionsWe propose a new hypothesis linking ecological, physiological, developmental and evolutionary processes to adumbrate a comprehensive explanation for the evolution of the lemur syndrome, whose assumptions and predictions can guide diverse future research on lemurs. This hypothesis should also encourage students of other behavioral phenomena to consider the potential role of developmental plasticity in evolutionary innovation.

Gene conversions are frequent but not under positive selection in the Siglec gene families of primates.

Siglecs are cell surface proteins that belong to the immunoglobulin superfamily and which bind sialic acids. They are composed of two groups, the conserved Siglecs and the CD33-related Siglecs. Previous studies have reported the occurrence of gene conversions between human CD33-related Siglecs and suggested that these conversions are adaptive because they increase the diversity of these immunoglobulin-related genes. Here, we analyze the Siglec genes of five primate species and show that gene conversions are not observed between conserved Siglec genes but that they are frequent between primate CD33-related Siglecs. The gene conversions between CD33-related Siglec genes only occur between similar genes and equally frequently in sialic acid binding and nonbinding domains. Furthermore, dN/dS ratio tests show that most of the Ig-like V-type 1 and the Ig-like C2-type 1 domains of Siglec genes evolve either neutrally or under purifying selection and that gene conversions were not responsible for the positively selected regions detected in the Ig-like V-type1 domain of the human SIGLEC7 and SIGLEC9 genes. Our results suggest that the frequent gene conversions between CD33-related Siglec genes are simply a consequence of the high degree of sequence similarity of these genes and that they are not adaptive.

Theories about evolutionary origins of human hepatitis B virus in primates and humans

IntroductionThe human hepatitis B virus causes acute and chronic hepatitis and is considered one of the most serious human health issues by the World Health Organization, causing thousands of deaths per year. There are similar viruses belonging to the Hepadnaviridae family that infect non-human primates and other mammals as well as some birds. The majority of non-human primate virus isolates were phylogenetically close to the human hepatitis B virus, but like the human genotypes, the origins of these viruses remain controversial. However, there is a possibility that human hepatitis B virus originated in primates. Knowing whether these viruses might be common to humans and primates is crucial in order to reduce the risk to humans. ObjectiveTo review the existing knowledge about the evolutionary origins of viruses of the Hepadnaviridae family in primates. MethodsThis review was done by reading several articles that provide information about the Hepadnaviridae virus family in non-human primates and humans and the possible origins and evolution of these viruses. ResultsThe evolutionary origin of viruses of the Hepadnaviridae family in primates has been dated back to several thousand years; however, recent analyses of genomic fossils of avihepadnaviruses integrated into the genomes of several avian species have suggested a much older origin of this genus. ConclusionSome hypotheses about the evolutionary origins of human hepatitis B virus have been debated since the ‘90s. One theory suggested a New World origin because of the phylogenetic co-segregation between some New World human hepatitis B virus genotypes F and H and woolly monkey human hepatitis B virus in basal sister-relationship to the Old World non-human primates and human hepatitis B virus variants. Another theory suggests an Old World origin of human hepatitis B virus, and that it would have been spread following prehistoric human migrations over 100,000 years ago. A third theory suggests a co-speciation of human hepatitis B virus in non-human primate hosts because of the proximity between the phylogeny of Old and New World non-human primate and their human hepatitis B virus variants. The importance of further research, related to the subject in South American wild fauna, is paramount and highly relevant for understanding the origin of human hepatitis B virus.

Pharmacological Inhibition of a MicroRNA Family in Nonhuman Primates by a Seed-Targeting 8-Mer AntimiR

MicroRNAs (miRNAs) regulate many aspects of human biology. They target mRNAs for translational repression or degradation through base pairing with 3' untranslated regions, primarily via seed sequences (nucleotides 2 to 8 in the mature miRNA sequence). A number of individual miRNAs and miRNA families share seed sequences and targets, but differ in the sequences outside of the seed. miRNAs have been implicated in the etiology of a wide variety of human diseases and therefore represent promising therapeutic targets. However, potential redundancy of different miRNAs sharing the same seed sequence and the challenge of simultaneously targeting miRNAs that differ significantly in nonseed sequences complicate therapeutic targeting approaches. We recently demonstrated effective inhibition of entire miRNA families using seed-targeting 8-mer locked nucleic acid (LNA)-modified antimiRs in short-term experiments in mammalian cells and in mice. However, the long-term efficacy and safety of this approach in higher organisms, such as humans and nonhuman primates, have not been determined. We show that pharmacological inhibition of the miR-33 family, key regulators of cholesterol/lipid homeostasis, by a subcutaneously delivered 8-mer LNA-modified antimiR in obese and insulin-resistant nonhuman primates results in derepression of miR-33 targets, such as ABCA1, increases circulating high-density lipoprotein cholesterol, and is well tolerated over 108 days of treatment. These findings demonstrate the efficacy and safety of an 8-mer LNA-antimiR against an miRNA family in a nonhuman primate metabolic disease model, suggesting that this could be a feasible approach for therapeutic targeting of miRNA families sharing the same seed sequence in human diseases.

Gene conversions are under purifying selection in the carcinoembryonic antigen immunoglobulin gene families of primates

The carcinoembryonic antigen (CEA) family contains a large number of glycoproteins belonging to the immunoglobulin superfamily. Here, we investigate whether the gene conversions occurring between primate CEA-related genes are adaptive. Our results show that primate CEA-related genes are subject to frequent and repeated gene conversion events. Furthermore, gene conversions occur most frequently between nearby genes sharing similar sequences, are not more frequent in Ig-like V-type 1 domains than in the Ig-like C2-type 1 domains and dN/dS ratio tests shown that both these domains evolve either neutrally or under purifying selection. Our results therefore suggest that CEA-related genes evolve under purifying selection and the frequent gene conversion events we observed likely represent selectively neutral events between genes having similar sequences and functions.

Bimodal evolution of the killer cell Ig-like receptor (KIR) family in New World primates

The immunoglobulin-like receptor (KIR) gene family in New World primates (Platyrrhini) has been characterized only in the owl monkey (Aotus sp.). To gain a better understanding of the KIR system in Platyrrhini, we analyzed a KIR haplotype in Ateles geoffroyi, and sequenced KIR complementary DNAs (cDNAs) from other three Atelidae species, Ateles hybridus, Ateles belzebuth, and Lagothrix lagotricha. Atelidae expressed a variable set of activating and inhibitory KIRs that diversified independently from their Catarrhini counterparts. They had a unique mechanism to generate activating receptors from inhibitory ones, involving a single nucleotide deletion in exon 7 and a change in the donor splice site of intron 7. The A. geoffroyi haplotype contained at least six gene models including a pseudogene, two coding inhibitory receptors, and three coding activating receptors. The centromeric region was in a tail-to-tail orientation with respect to the telomeric region. The owl monkey KIR haplotype shared this organization, and in phylogenetic trees, the centromeric genes clustered together with those of A. geoffroyi, whereas their telomeric genes clustered independently. KIR cDNAs from the other Atelidae species conformed to this pattern. Signatures of positive selection were found in residues predicted to interact with the major histocompatibility complex. Such signatures, however, primarily explained variability between paralogous genes but not between alleles in a locus. Atelidae, therefore, has expanded the KIR family in a bimodal fashion, where an inverted centromeric region has remained relatively conserved and the telomeric region has diversified by a rapid process of gene duplication and divergence, likely favored by positive selection for ligand binding.

Uniquely derived upper molar morphology of Eocene Amphipithecidae (Primates: Anthropoidea): Homology and phylogeny

The extinct Southeast Asian primate family Amphipithecidae is regularly cited in discussions of anthropoid origins, but its phylogenetic position remains controversial. In part, the lack of consensus regarding amphipithecid relationships can be attributed to uncertainty regarding the homology of upper molar structures in this group. Here, we describe a virtually pristine upper molar of Pondaungia cotteri from the late middle Eocene Pondaung Formation of Myanmar, which is the first example of a relatively unworn and well-preserved amphipithecid upper molar ever recovered. The distolingual upper molar cusp in this new specimen of Pondaungia appears to be a lingually displaced and enlarged metaconule, rather than a hypocone or pseudohypocone as previous workers have thought. Reassessment of the upper molar morphology of other amphipithecids and putative amphipithecids reveals a very similar pattern in Siamopithecus, Myanmarpithecus and Ganlea, all of which are interpreted as having upper molars showing many of the same derived features apparent in Pondaungia. In contrast, the upper molar morphology of Bugtipithecus diverges radically from that of undoubted amphipithecids, and the latter taxon is excluded from Amphipithecidae on this basis. Phylogenetic analyses of several character–taxon matrices culled from the recent literature and updated to reflect the new information on amphipithecid upper molar morphology yield similar results. Consensus tree topologies derived from these analyses support amphipithecid monophyly and stable relationships within Amphipithecidae. Amphipithecids appear to be stem members of the anthropoid clade.

Developmental constraints on behavioural flexibility

We suggest that variation in mammalian behavioural flexibility not accounted for by current socioecological models may be explained in part by developmental constraints. From our own work, we provide examples of constraints affecting variation in behavioural flexibility, not only among individuals, but also among species and higher taxonomic units. We first implicate organizational maternal effects of androgens in shaping individual differences in aggressive behaviour emitted by female spotted hyaenas throughout the lifespan. We then compare carnivores and primates with respect to their locomotor and craniofacial adaptations. We inquire whether antagonistic selection pressures on the skull might impose differential functional constraints on evolvability of skulls and brains in these two orders, thus ultimately affecting behavioural flexibility in each group. We suggest that, even when carnivores and primates would theoretically benefit from the same adaptations with respect to behavioural flexibility, carnivores may nevertheless exhibit less behavioural flexibility than primates because of constraints imposed by past adaptations in the morphology of the limbs and skull. Phylogenetic analysis consistent with this idea suggests greater evolutionary lability in relative brain size within families of primates than carnivores. Thus, consideration of developmental constraints may help elucidate variation in mammalian behavioural flexibility.

Pregnancy-Specific Glycoproteins Bind Integrin αIIbβ3 and Inhibit the Platelet—Fibrinogen Interaction

Pregnancy-specific glycoproteins (PSGs) are immunoglobulin superfamily members encoded by multigene families in rodents and primates. In human pregnancy, PSGs are secreted by the syncytiotrophoblast, a fetal tissue, and reach a concentration of up to 400 ug/ml in the maternal bloodstream at term. Human and mouse PSGs induce release of anti-inflammatory cytokines such as IL-10 and TGFβ1 from monocytes, macrophages, and other cell types, suggesting an immunoregulatory function. RGD tri-peptide motifs in the majority of human PSGs suggest that they may function like snake venom disintegrins, which bind integrins and inhibit interactions with ligands. We noted that human PSG1 has a KGD, rather than an RGD motif. The presence of a KGD in barbourin, a platelet integrin αIIbβ3 antagonist found in snake venom, suggested that PSG1 may be a selective αIIbβ3 ligand. Here we show that human PSG1 binds αIIbβ3 and inhibits the platelet – fibrinogen interaction. Unexpectedly, however, the KGD is not critical as multiple PSG1 domains independently bind and inhibit αIIbβ3 function. Human PSG9 and mouse Psg23 are also inhibitory suggesting conservation of this function across primate and rodent PSG families. Our results suggest that in species with haemochorial placentation, in which maternal blood is in direct contact with fetal trophoblast, the high expression level of PSGs reflects a requirement to antagonise abundant (3 mg/ml) fibrinogen in the maternal circulation, which may be necessary to prevent platelet aggregation and thrombosis in the prothrombotic maternal environment of pregnancy.

Dynamic Actin Gene Family Evolution in Primates

Actin is one of the most highly conserved proteins and plays crucial roles in many vital cellular functions. In most eukaryotes, it is encoded by a multigene family. Although the actin gene family has been studied a lot, few investigators focus on the comparison of actin gene family in relative species. Here, the purpose of our study is to systematically investigate characteristics and evolutionary pattern of actin gene family in primates. We identified 233 actin genes in human, chimpanzee, gorilla, orangutan, gibbon, rhesus monkey, and marmoset genomes. Phylogenetic analysis showed that actin genes in the seven species could be divided into two major types of clades: orthologous group versus complex group. Codon usages and gene expression patterns of actin gene copies were highly consistent among the groups because of basic functions needed by the organisms, but much diverged within species due to functional diversification. Besides, many great potential pseudogenes were found with incomplete open reading frames due to frameshifts or early stop codons. These results implied that actin gene family in primates went through “birth and death” model of evolution process. Under this model, actin genes experienced strong negative selection and increased the functional complexity by reproducing themselves.

Application of Systems Biology and Bioinformatics Methods in Biochemistry and Biomedicine

Application of Systems Biology and Bioinformatics Methods in Biochemistry and Biomedicine