Primate Evolution Research Articles

Unusual sequence characteristics of human chromosome 19 are conserved across 11 nonhuman primates

BackgroundHuman chromosome 19 has many unique characteristics including gene density more than double the genome-wide average and 20 large tandemly clustered gene families. It also has the highest GC content of any chromosome, especially outside gene clusters. The high GC content and concomitant high content of hypermutable CpG sites raises the possibility chromosome 19 exhibits higher levels of nucleotide diversity both within and between species, and may possess greater variation in DNA methylation that regulates gene expression.ResultsWe examined GC and CpG content of chromosome 19 orthologs across representatives of the primate order. In all 12 primate species with suitable genome assemblies, chromosome 19 orthologs have the highest GC content of any chromosome. CpG dinucleotides and CpG islands are also more prevalent in chromosome 19 orthologs than other chromosomes. GC and CpG content are generally higher outside the gene clusters. Intra-species variation based on SNPs in human common dbSNP, rhesus, crab eating macaque, baboon and marmoset datasets is most prevalent on chromosome 19 and its orthologs. Inter-species comparisons based on phyloP conservation show accelerated nucleotide evolution for chromosome 19 promoter flanking and enhancer regions. These same regulatory regions show the highest CpG density of any chromosome suggesting they possess considerable methylome regulatory potential.ConclusionsThe pattern of high GC and CpG content in chromosome 19 orthologs, particularly outside gene clusters, is present from human to mouse lemur representing 74 million years of primate evolution. Much CpG variation exists both within and between primate species with a portion of this variation occurring in regulatory regions.

The postnatal development of MT, V1, LGN, pulvinar and SC in prosimian galagos (Otolemur garnettii).

Considerable evidence supports the premise that the visual system of primates develops hierarchically, with primary visual cortex developing structurally and functionally first, thereby influencing the subsequent development of higher cortical areas. An apparent exception is the higher order middle temporal visual area (MT), which appears to be histologically distinct near the time of birth in marmosets. Here we used a number of histological and immunohistological markers to evaluate the maturation of cortical and subcortical components of the visual system in galagos ranging from newborns to adults. Galagos are representative of the large strepsirrhine branch of primate evolution, and studies of these primates help identify brain features that are broadly similar across primate taxa. The histological results support the view that MT is functional at or near the time of birth, as is primary visual cortex. Likewise, the superior colliculus, dorsal lateral geniculate nucleus, and the posterior nucleus of the pulvinar are well-developed by birth. Thus, these subcortical structures likely provide visual information directly or indirectly to cortex in newborn galagos. We conclude that MT resembles a primary sensory area by developing early, and that the early development of MT may influence the subsequent development of dorsal stream visual areas.

Cognitive control of orofacial motor and vocal responses in the ventrolateral and dorsomedial human frontal cortex

In the primate brain, a set of areas in the ventrolateral frontal (VLF) cortex and the dorsomedial frontal (DMF) cortex appear to control vocalizations. The basic role of this network in the human brain and how it may have evolved to enable complex speech remain unknown. In the present functional neuroimaging study of the human brain, a multidomain protocol was utilized to investigate the roles of the various areas that comprise the VLF-DMF network in learning rule-based cognitive selections between different types of motor actions: manual, orofacial, nonspeech vocal, and speech vocal actions. Ventrolateral area 44 (a key component of the Broca's language production region in the human brain) is involved in the cognitive selection of orofacial, as well as, speech and nonspeech vocal responses; and the midcingulate cortex is involved in the analysis of speech and nonspeech vocal feedback driving adaptation of these responses. By contrast, the cognitive selection of speech vocal information requires this former network and the additional recruitment of area 45 and the presupplementary motor area. We propose that the basic function expressed by the VLF-DMF network is to exert cognitive control of orofacial and vocal acts and, in the language dominant hemisphere of the human brain, has been adapted to serve higher speech function. These results pave the way to understand the potential changes that could have occurred in this network across primate evolution to enable speech production.

Widespread correlation of KRAB zinc finger protein binding with brain-developmental gene expression patterns.

The large family of KRAB zinc finger (KZNF) genes are transcription factors implicated in recognizing and repressing repetitive sequences such as transposable elements (TEs) in our genome. Through successive waves of retrotransposition-mediated insertions, various classes of TEs have invaded mammalian genomes at multiple timepoints throughout evolution. Even though most of the TE classes in our genome lost the capability to retrotranspose millions of years ago, it remains elusive why the KZNFs that evolved to repress them are still retained in our genome. One hypothesis is that KZNFs become repurposed for other regulatory roles. Here, we find evidence that evolutionary changes in KZNFs provide them not only with the ability to repress TEs, but also to bind to gene promoters independent of TEs. Using KZNF binding site data in conjunction with gene expression values from the Allen Brain Atlas, we show that KZNFs have the ability to regulate gene expression in the human brain in a region-specific manner. Our analysis shows that the expression of KZNFs shows correlation with the expression of their target genes, suggesting that KZNFs have a direct influence on gene expression in the developing human brain. The extent of this regulation and the impact it has on primate brain evolution are still to be determined, but our results imply that KZNFs have become widely integrated into neuronal gene regulatory networks. Our analysis predicts that gene expression networks have been repeatedly innovated throughout primate evolution, continuously gaining new layers of gene regulation mediated by both TEs and KZNFs in our genome. This article is part of a discussion meeting issue 'Crossroads between transposons and gene regulation'.

Biological convergence of three human and animal model quantitative trait loci for blood pressure.

Blood pressure (BP) is comparable among different mammalian orders, despite their evolution divergence. Because of it, fundamental mechanisms should connect humans and rodents by their shared BP physiology. We hypothesized that similar quantitative trait loci (QTLs) function in both humans and rodents in controlling BP. We utilized inbred hypertensive Dahl salt-sensitive rats (DSS) as a functional proxy to evaluate the relevance of human genome-wide association studies (GWAS) genes in BP regulation. First, three DSS BP QTLs functionally captured three specific human GWAS genes. Each QTL has a major biological impact, not a miniscule effect, on BP, in causation by function. Second, noncoding single-nucleotide polymorphisms (SNPs) found in GWAS are by products of primate evolution, instead of mechanistic drivers in regulating BP, because their absence did not impact on BP of mammals. Third, a missense mutation, rather than a noncoding GWAS SNP marking it nearby, is the priority functional basis for a given QTL. Depleting such a noncoding GWAS SNP had no impact, whereas eliminating the muscarinic cholinergic receptor 3 (M3R) signaling decreased BP. Finally, epistatic modularity biologically organizes multiple QTLs with redundant functions, and is the genetic mechanism that modulates the BP homeostasis when QTLs function collectively. Two pathogenic pathways of hypertension biologically unify mechanisms of BP regulations for humans and their functional surrogates. The mechanism-based biology for the M3R-mediated pathway in raising BP has established M3R as a novel pathogenesis-driven target for antihypertension therapies.

First navicular remains of a European adapiform (Anchomomys frontanyensis) from the Middle Eocene of the Eastern Pyrenees (Catalonia, Spain): implications for early primate locomotor behavior and navicular evolution

We describe the first known navicular bones for an Eocene euprimate from Europe and assess their implications for early patterns of locomotor evolution in primates. Recovered from the fossil site of Sant Jaume de Frontanyà-3C (Barcelona, Spain), the naviculars are attributed to Anchomomys frontanyensis. The small size of A. frontanyensis allows us to consider behavioral implications of comparisons with omomyiforms, regardless of allometric sources of navicular variation. Researchers usually consider omomyiforms to be more prone to leaping than contemporaneous adapiforms partly because of the more pronounced elongation of omomyiform tarsal elements. However, A. frontanyensis differs from other adapiforms and is similar to some omomyiforms in its more elongated navicular proportions. Although this might raise questions about attribution of these naviculars to A. frontanyensis, the elements exhibit clear strepsirrhine affinities leaving little doubt about the attribution: the bones' mesocuneiform facets contact their cuboid facets. We further propose that this strepsirrhine-specific feature in A. frontanyensis and other adapiforms reflects use of more inverted foot postures and potentially smaller substrates than sympatric omomyiforms that lack it. Thus substrate differences may have influenced niche partitioning in Eocene euprimate communities along with differences in locomotor agility. As previous studies on the astragalus and the calcaneus have suggested, this study on the navicular is consistent with the hypothesis that the locomotor mode of A. frontanyensis was similar to that of extant cheirogaleids, especially species of Microcebus and Mirza.

Hominin-specific regulatory elements selectively emerged in oligodendrocytes and are disrupted in autism patients

Speciation is associated with substantial rewiring of the regulatory circuitry underlying the expression of genes. Determining which changes are relevant and underlie the emergence of the human brain or its unique susceptibility to neural disease has been challenging. Here we annotate changes to gene regulatory elements (GREs) at cell type resolution in the brains of multiple primate species spanning most of primate evolution. We identify a unique set of regulatory elements that emerged in hominins prior to the separation of humans and chimpanzees. We demonstrate that these hominin gains perferentially affect oligodendrocyte function postnatally and are preferentially affected in the brains of autism patients. This preference is also observed for human-specific GREs suggesting this system is under continued selective pressure. Our data provide a roadmap of regulatory rewiring across primate evolution providing insight into the genomic changes that underlie the emergence of the brain and its susceptibility to neural disease.

Aberrantly High Levels of Somatic LINE-1 Expression and Retrotransposition in Human Neurological Disorders.

Retrotransposable elements (RTEs) have actively multiplied over the past 80 million years of primate evolution, and as a consequence, such elements collectively occupy ∼ 40% of the human genome. As RTE activity can have detrimental effects on the human genome and transcriptome, silencing mechanisms have evolved to restrict retrotransposition. The brain is the only known somatic tissue where RTEs are de-repressed throughout the life of a healthy human and each neuron in specific brain regions accumulates up to ∼13.7 new somatic L1 insertions (and perhaps more). However, even higher levels of somatic RTE expression and retrotransposition have been found in a number of human neurological disorders. This review is focused on how RTE expression and retrotransposition in neuronal tissues might contribute to the initiation and progression of these disorders. These disorders are discussed in three broad and sometimes overlapping categories: 1) disorders such as Rett syndrome, Aicardi-Goutières syndrome, and ataxia–telangiectasia, where expression/retrotransposition is increased due to mutations in genes that play a role in regulating RTEs in healthy cells, 2) disorders such as autism spectrum disorder, schizophrenia, and substance abuse disorders, which are thought to be caused by a combination of genetic and environmental stress factors, and 3) disorders associated with age, such as frontotemporal lobar degeneration (FTLD), amyotrophic lateral sclerosis (ALS), and normal aging, where there is a time-dependent accumulation of neurological degeneration, RTE copy number, and phenotypes. Research has revealed increased levels of RTE activity in many neurological disorders, but in most cases, a clear causal link between RTE activity and these disorders has not been well established. At the same time, even if increased RTE activity is a passenger and not a driver of disease, a detrimental effect is more likely than a beneficial one. Thus, a better understanding of the role of RTEs in neuronal tissues likely is an important part of understanding, preventing, and treating these disorders.

Asymmetrical gait kinematics of free-ranging callitrichine primates in response to changes in substrate diameter and orientation.

Arboreal environments present considerable biomechanical challenges for animals moving and foraging among substrates varying in diameter, orientation and compliance. Most studies of quadrupedal gait kinematics in primates and other arboreal mammals have focused on symmetrical walking gaits and the significance of diagonal sequence gaits. Considerably less research has examined asymmetrical gaits, despite their prevalence in small-bodied arboreal taxa. Here, we examined whether and how free-ranging callitrichine primates adjust asymmetrical gait kinematics to changes in substrate diameter and orientation, as well as how variation in gait kinematics affects substrate displacement. We used high-speed video to film free-ranging Saguinus tripartitus and Cebuella pygmaea inhabiting the Tiputini Biodiversity Station, Ecuador. We found that S. tripartitus used bounding and half-bounding gaits on larger substrates versus gallops and symmetrical gaits on smaller substrates, and also shifted several kinematic parameters consistent with attenuating forces transferred from the animal to the substrate. Similarly, C. pygmaea shifted from high-impact bounding gaits on larger substrates to using more half-bounding gaits on smaller substrates; however, kinematic adjustments to substrate diameter were not as profound as in S. tripartitus Both species adjusted gait kinematics to changes in substrate orientation; however, gait kinematics did not significantly affect empirical measures of substrate displacement in either species. Because of their small body size, claw-like nails and reduced grasping capabilities, callitrichines arguably represent extant biomechanical analogs for an early stage in primate evolution. As such, greater attention should be placed on understanding asymmetrical gait dynamics for insight into hypotheses concerning early primate locomotor evolution. .

The Evolution of the Pulvinar Complex in Primates and Its Role in the Dorsal and Ventral Streams of Cortical Processing.

Current evidence supports the view that the visual pulvinar of primates consists of at least five nuclei, with two large nuclei, lateral pulvinar ventrolateral (PLvl) and central lateral nucleus of the inferior pulvinar (PIcl), contributing mainly to the ventral stream of cortical processing for perception, and three smaller nuclei, posterior nucleus of the inferior pulvinar (PIp), medial nucleus of the inferior pulvinar (PIm), and central medial nucleus of the inferior pulvinar (PIcm), projecting to dorsal stream visual areas for visually directed actions. In primates, both cortical streams are highly dependent on visual information distributed from primary visual cortex (V1). This area is so vital to vision that patients with V1 lesions are considered “cortically blind”. When the V1 inputs to dorsal stream area middle temporal visual area (MT) are absent, other dorsal stream areas receive visual information relayed from the superior colliculus via PIp and PIcm, thereby preserving some dorsal stream functions, a phenomenon called “blind sight”. Non-primate mammals do not have a dorsal stream area MT with V1 inputs, but superior colliculus inputs to temporal cortex can be more significant and more visual functions are preserved when V1 input is disrupted. The current review will discuss how the different visual streams, especially the dorsal stream, have changed during primate evolution and we propose which features are retained from the common ancestor of primates and their close relatives.

Geographical patterns and current and short‐term historical correlates of phylogenetic diversity and endemism for New World primates

AbstractAimAddressing the phylogenetic relationship among species has been insightful to understand evolutionary and biogeographical processes shaping the distribution of diversity across broad geographical gradients. Here we determine the geographical distribution and the variables correlated with the phylogenetic component of diversity and endemism for primates, as well as their relationships with the taxonomic component of diversity.LocationNew World.TaxonNew World monkeys, Platyrrhini.MethodsWe mapped primate occurrence in cells of 110 × 110 km. For each cell, we calculated phylogenetic diversity (PD) and endemism (PE), as well as how much these indices deviate from their expected values based on species richness (SR) and endemism (SE), respectively. Using simultaneous autoregressive models, we tested the effects of mean annual temperature, forest structure and climate history on the current patterns of primate phylogenetic diversity.ResultsWe found that most primate phylogenetic diversity is found in the tropical forests of South America. Tropical forests also present much higher PD and PE than predicted by SR and SE, respectively, demonstrating their importance in producing and maintaining primate phylogenetic diversity in the New World. Furthermore, regions presenting low SR and SE nevertheless show high PE, likely because these areas have witnessed the evolution of many clades occurring exclusively therein. Overall, mean annual temperature had the highest influence in explaining phylogenetic indices.Main conclusionsOur results suggest a strong influence of primate biogeography throughout the New World on the geographical distribution of the phylogenetic component of their diversity, with the Amazon, Atlantic Forest and Central America containing the greatest amount and endemism of phylogenetic diversity. Our study contributes to a better understanding of the dynamics underlying the geographical distribution of New World's primate diversity, especially in a phylogenetic context in which their biogeographical history has deeply affected current patterns of primate diversity in this region. Our results provide essential information for the conservation of primate evolutionary history, especially considering the forecast effects of habitat loss and climate change on the dynamics of tropical forests.

Evolutionary transitions toward pair living in nonhuman primates as stepping stones toward more complex societies.

Nonhuman primate societies vary tremendously in size and composition, but how and why evolutionary transitions among different states occurred remains highly controversial. In particular, how many times pair living evolved and the social states of the ancestors of pair- and group-living species remains contentious. We examined evolutionary transitions in primate social evolution by using new, independent categorizations of sociality and different phylogenetic hypotheses with a vastly expanded dataset. Using Bayesian phylogenetic comparative methods, we consistently found the strongest support for a model that invokes frequent transitions between solitary ancestors and pair-living descendants, with the latter giving rise to group-living species. This result was robust to systematic variation in social classification, sample size, and phylogeny. Our analyses therefore indicate that pair living was a stepping stone in the evolution of structurally more complex primate societies, a result that bolsters the role of kin selection in social evolution.

Evolutionary shifts dramatically reorganized the human hippocampal complex.

The hippocampal complex (HC) is central to long-term memory storage and retrieval as well as spatial navigation across many species. Notably, humans appear to have greatly enhanced and possibly unique HC-mediated capacities such as constructive episodic simulation. Key studies have shown that the human HC is disproportionately large amongst hominoids, but much remains unknown at the levels of substructural evolutionary reorganization and ecological selection. Here, we calculated relative sizes of 12 HC subregions in a diverse sample of 44 primate species. We then used a Bayesian phylogenetic method, selective regime analysis, to identify 27 separate evolutionary shifts in HC organization across 65 million years of primate evolution. Additionally, a series of multivariate phylogenetic regressions using HC-related ecological variables as predictors (Diet Breadth, Population Density, Group Size, Home Range Size, and Residual Home Range) revealed that relative fascia dentata and CA1 size were both significantly predicted by species' home range size (after correcting for body size). However, perhaps the most notable finding of this study was that the shifts in HC size and subregional organization in the human lineage were the largest seen in all of primate evolution, rendering modern humans with a HC that is a clear outlier amongst all nonhuman primates investigated here. Given the extensive literature confirming the relationship between HC organization and function, these selective shifts are likely to have played a significant role in the emergence of human-specific capacities, such as constructive episodic simulation.

A digital collection of rare and endangered lemurs and other primates from the Duke Lemur Center.

Scientific study of lemurs, a group of primates found only on Madagascar, is crucial for understanding primate evolution. Unfortunately, lemurs are among the most endangered animals in the world, so there is a strong impetus to maximize as much scientific data as possible from available physical specimens. MicroCT scanning efforts at Duke University have resulted in scans of more than 100 strepsirrhine cadavers representing 18 species from the Duke Lemur Center. An error study of the microCT scanner recovered less than 0.3% error at multiple resolution levels. Scans include specimen overviews and focused, high-resolution selections of complex anatomical regions (e.g., cranium, hands, feet). Scans have been uploaded to MorphoSource, an online digital repository for 3D data. As captive (but free ranging) individuals, these specimens have a wealth of associated information that is largely unavailable for wild populations, including detailed life history data. This digital collection maximizes the information obtained from rare and endangered animals with minimal degradation of the original specimens.

The gaits of marsupials and the evolution of diagonal-sequence walking in primates.

Documenting the variety of quadrupedal walking gaits in a variety of marsupials (arboreal vs. terrestrial, with and without grasping hind feet), to aid in developing and refining a general theory of gait evolution in primates. Video records of koalas, ringtail possums, tree kangaroos, sugar gliders, squirrel gliders, wombats, numbats, quolls, a thylacine, and an opossum walking on a variety of substrates were made and analyzed to derive duty factors and diagonalities for symmetrical walking gaits. The resulting distributions of data points were compared with published data and theories. Terrestrial marsupials' gaits overwhelmingly plot slightly below the theoretical "horse line" (Cartmill et al., Zoological Journal of the Linnean Society. 2002;136:401-420) typical of terrestrial mammals; arboreal marsupials' gaits overwhelmingly plot more decisively above it. Both distributions are roughly parallel to the horse line, but arboreal animals exhibit increased diagonality, so that their higher-speed walking gaits overlap with those of typical primates on the Hildebrand diagram of diagonality against duty factor. Quadrupeds avoid gaits lying exactly on the (theoretically optimum) horse line, to avoid fore/hind limb interference ("forging"). This can be accomplished by either a slight reduction in diagonality ("downshifting") or a more decisive increase ("upshifting"). Tree-dwellers adopt the second option to eliminate unilateral bipods of support from the gait cycle. The upshifted horse line represents an early phase in the evolution of primate-like diagonal-sequence gaits.

Primates got personality, too: Toward an integrative primatology of consistent individual differences in behavior.

In recent years, research on animal personality has exploded within the field of behavioral ecology. Consistent individual differences in behavior exist in a wide range of species, and these differences can have fitness consequences and influence several aspects of a species' ecology. In comparison to studies of other animals, however, there has been relatively little research on the behavioral ecology of primate personality. This is surprising given the large body of research within psychology and biomedicine showing that primate personality traits are heritable and linked to health and life history outcomes. In this article, I bring together theoretical perspectives on the ecology and evolution of animal personality with an integrative review of what we know about primate personality from studies conducted on captive, free-ranging, and wild primates. Incorporating frameworks that emphasize consistency in behavior into primate behavioral ecology research holds promise for improving our understanding of primate behavioral evolution.

Early anthropoid femora reveal divergent adaptive trajectories in catarrhine hind-limb evolution

The divergence of crown catarrhines—i.e., the split of cercopithecoids (Old World monkeys) from hominoids (apes and humans)—is a poorly understood phase in our shared evolutionary history with other primates. The two groups differ in the anatomy of the hip joint, a pattern that has been linked to their locomotor strategies: relatively restricted motion in cercopithecoids vs. more eclectic movements in hominoids. Here we take advantage of the first well-preserved proximal femur of the early Oligocene stem catarrhine Aegyptopithecus to investigate the evolution of this anatomical region using 3D morphometric and phylogenetically-informed evolutionary analyses. Our analyses reveal that cercopithecoids and hominoids have undergone divergent evolutionary transformations of the proximal femur from a similar ancestral morphology that is not seen in any living anthropoid, but is preserved in Aegyptopithecus, stem platyrrhines, and stem cercopithecoids. These results highlight the relevance of fossil evidence for illuminating key adaptive shifts in primate evolution.

Macroevolutionary trends of brain mass in Primates

AbstractA distinctive trait in primate evolution is the expansion in brain mass. The potential drivers of this trend and how and whether encephalization influenced diversification dynamics in this group are hotly debated. We assembled a phylogeny accounting for 317 primate species, including both extant and extinct taxa, to identify macroevolutionary trends in brain mass evolution. Our findings show that Primates as a whole follow a macroevolutionary trend for an increase in body mass, relative brain mass and speciation rate over time. Although the trend for increased encephalization (brain mass) applies to all Primates, hominins stand out for their distinctly higher rates. Within hominins, this unique trend applies linearly over time and starts with Australopithecus africanus. The increases in both speciation rate and encephalization begin in the Oligocene, suggesting the two variables are causally associated. The substitution of early, stem Primates belonging to plesiadapiforms with crown Primates seems to be responsible for these macroevolutionary trends. However, our findings also suggest that cognitive capacities favoured speciation in hominins.

Emerging Roles of Long Non-Coding RNAs as Drivers of Brain Evolution.

Mammalian genomes encode tens of thousands of long-noncoding RNAs (lncRNAs), which are capable of interactions with DNA, RNA and protein molecules, thereby enabling a variety of transcriptional and post-transcriptional regulatory activities. Strikingly, about 40% of lncRNAs are expressed specifically in the brain with precisely regulated temporal and spatial expression patterns. In stark contrast to the highly conserved repertoire of protein-coding genes, thousands of lncRNAs have newly appeared during primate nervous system evolution with hundreds of human-specific lncRNAs. Their evolvable nature and the myriad of potential functions make lncRNAs ideal candidates for drivers of human brain evolution. The human brain displays the largest relative volume of any animal species and the most remarkable cognitive abilities. In addition to brain size, structural reorganization and adaptive changes represent crucial hallmarks of human brain evolution. lncRNAs are increasingly reported to be involved in neurodevelopmental processes suggested to underlie human brain evolution, including proliferation, neurite outgrowth and synaptogenesis, as well as in neuroplasticity. Hence, evolutionary human brain adaptations are proposed to be essentially driven by lncRNAs, which will be discussed in this review.

Cooperative evolution of two different TEs results in lineage-specific novel transcripts in the BLOC1S2 gene

BackgroundThe BLOC1S2 gene encodes the multifunctional protein BLOS2, a shared subunit of two lysosomal trafficking complexes: i) biogenesis of lysosome-related organelles complex-1 and i) BLOC-1-related complex. In our previous study, we identified an intriguing unreported transcript of the BLOC1S2 gene that has a novel exon derived from two transposable elements (TEs), MIR and AluSp. To investigate the evolutionary footprint and molecular mechanism of action of this transcript, we performed PCR and RT-PCR experiments and sequencing analyses using genomic DNA and RNA samples from humans and various non-human primates.ResultsThe results showed that the MIR element had integrated into the genome of our common ancestor, specifically in the BLOC1S2 gene region, before the radiation of all primate lineages and that the AluSp element had integrated into the genome of our common ancestor, fortunately in the middle of the MIR sequences, after the divergence of Old World monkeys and New World monkeys. The combined MIR and AluSp sequences provide a 3′ splice site (AG) and 5′ splice site (GT), respectively, and generate the Old World monkey-specific transcripts. Moreover, branch point sequences for the intron removal process are provided by the MIR and AluSp combination.ConclusionsWe show for the first time that sequential integration into the same location and sequence divergence events of two different TEs generated lineage-specific transcripts through sequence collaboration during primate evolution.