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Propagation of tool use in primates?

Propagation of tool use in primates?


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There are several famous cases of great apes demonstrating a surprising degree of wherewithal in communication and tool use - even monkeys can learn some tool use from each other observationally, even if "teaching" would be an exaggeration.

The ready availability of this information will preclude me from bothering to cite a palate of examples.

Has anyone ever considered, as an experiment, taking such primates which display exemplary tool use in the lab and (at least partially) reintroducing them into the wild and seeing if (perhaps specially crafted) tool lessons learned form us humans propagates among their fellows?

If not, why not?


Use of Tools by Wild Macaque Monkeys in Singapore

ALL known reports of tool use in wild and captive primates have been listed in two reviews 1,2 . Whereas agonistic tool using has been reported in many species of primates, observations of non-agonistic tool use by wild primates are surprisingly rare. Of the eleven reports of such tool use cited by Kortlandt and Kooij 2 , six involved apes, and of the others concerning monkeys, only one instance of the cleaning of food with leaves or other material is mentioned. A squirrel monkey swept the food over the ground with a stick, to dislodge ants. There are very few known reports of such treatment of food before eating. Crook (personal communication) has observed the cleaning of prickly pear (Opuntia) fruit by Doguera baboons, Papio doguera, in Ethiopia. The fruits are often rolled to and fro on patches of dry earth—evidently to remove the spines. Vevers and Weiner 3 discussed the use of a heavy bone by a captive Capuchin to crack nuts. Kawamura 4 has described the “sub-culture propagation” of potato washing in a troop of Japanese macaques, Macaca fuscata.


The ecology of primate material culture

Tool use in extant primates may inform our understanding of the conditions that favoured the expansion of hominin technology and material culture. The ‘method of exclusion’ has, arguably, confirmed the presence of culture in wild animal populations by excluding ecological and genetic explanations for geographical variation in behaviour. However, this method neglects ecological influences on culture, which, ironically, may be critical for understanding technology and thus material culture. We review all the current evidence for the role of ecology in shaping material culture in three habitual tool-using non-human primates: chimpanzees, orangutans and capuchin monkeys. We show that environmental opportunity, rather than necessity, is the main driver. We argue that a better understanding of primate technology requires explicit investigation of the role of ecological conditions. We propose a model in which three sets of factors, namely environment, sociality and cognition, influence invention, transmission and retention of material culture.

1. Introduction

Tool use is widespread in the animal kingdom [1], but habitual tool use is restricted to only a few bird and mammal species, such as New Caledonian crows (Corvus moneduloides) and bottle-nosed dolphins (Tursiops sp.) [1]. Among non-human primates, frequent and diverse tool use is observed only in chimpanzees (Pan troglodytes) [2], orangutans (Pongo pygmaeus and Pongo abelii) [3], bearded capuchins (Sapajus libidinosus) [4] and, to a lesser extent, long-tailed macaques (Macaca fascicularis aurea) [5]. Given their close phylogenetic relatedness to humans, their tool use may provide insights into the conditions that favoured the extraordinary expansion of hominin technology.

Chimpanzees use a variety of tools in a range of contexts, including foraging, self-maintenance and social functions [2]. Orangutans use stick tools in similar contexts, especially on Sumatra [3]. Wild bearded capuchin monkeys living in savannah-like environments also use a variety of tools, including stones to crack open nuts and sticks to dig for tubers [4]. Lastly, island-dwelling long-tailed macaques use stones to crack molluscs, crabs and nuts [6].

The question is whether the use of tools in these primates can be termed ‘cultural’. It is important to resolve this question, because human technology is intrinsically cultural, as both the spread and maintenance of technological skills and knowledge are strongly dependent on social transmission [7].

The principal method used in wild animals to establish culture in nature has been the ‘method of exclusion’ [3,8]. This method identifies geographically variable behaviour patterns across long-term study sites and seeks to establish the presence of cultural variants by excluding behavioural variants that can be attributed to genetic or ecological differences across sites. This method has been used to demonstrate the presence of culture in wild populations, including chimpanzees and orangutans [3,8].

The main weakness of this method is that it cannot rule out ecology as an alternative explanation for behavioural variation [9]. Because unrecognized ecological differences may induce individuals to adopt different behavioural variants in the absence of any social transmission, this method has been applied as conservatively as possible by removing all variants with ecological correlates. However, as an unfortunate side effect, behavioural variants that have ecological (or genetic) correlates but are nonetheless culturally acquired will not be recognized as such. Importantly, social learning allows individuals to acquire behaviours appropriate to their ecological conditions, which implies that some important socially learned behaviours will be linked to the local environment.

In this opinion piece, we show how ecology affects primate material culture by influencing innovation, transmission and retention of tool-use behaviours in a population. We review findings on the influence of ecology on material culture in three habitual tool-using non-human primates: chimpanzees, orangutans and capuchin monkeys. By considering how not just social organization and cognitive capacities, but also the environment influence primate tool use [10], we may begin to disentangle the different determinants of material culture in non-human primates as well as humans. We conclude by presenting directions for future research and by providing a model describing the factors driving the evolution of primate material culture.

2. Ecology of culture matters

In line with the idea that necessity is the mother of invention, a link between fruit scarcity and an increase in certain types of tool use has been described for one chimpanzee population at Bossou, Guinea [11]. Similarly, a relationship between tool use and seasonal food scarcity has been suggested for bearded capuchins [12] and long-tailed macaques [6], although in neither case was an assessment of food availability carried out. Moreover, none of these studies tested alternative ecological hypotheses to explain tool-use patterns.

A number of recent studies [13–15] have explicitly addressed the role of ecological conditions in shaping primate foraging tool use by testing two main, not mutually exclusive, hypotheses [16]. The opportunity hypothesis states that encounter rates with tool materials and resources whose exploitation requires tools affect the likelihood of tool invention and frequency of tool use, thus explaining tool-use patterns. In contrast, the necessity hypothesis states that tool use is a response to scarcity of (preferred) foods [16,17]. As there is now overwhelming evidence from wild and captive studies that tool use in primates is socially learned [18], the following cases are assumed to be culturally transmitted.

For chimpanzees, the opportunity hypothesis was supported at Seringbara, Guinea, where they use tools to harvest widely available army ants, but not to fish termites from rare and peripheral Macrotermes mounds [13]. Moreover, altitudinal overlap with ants, but not with termites, further increased opportunities to encounter ants (figure 1a and the electronic supplementary material, S1). In addition, at sites with higher (total) nut tree densities, chimpanzees were more likely to use tools to crack nuts (figure 1b and the electronic supplementary material, S1). The necessity hypothesis was not supported at Seringbara, as tool use in ant feeding did not increase at times of fruit scarcity (figure 1g and the electronic supplementary material, S1). Similarly, chimpanzees at Goualougo, Congo, did not compensate for seasonal lack of fruit by increasing tool use for harvesting social insects or honey [15]. Moreover, there was no correlation between the intensity of seasonality and the number of subsistence tool-use variants across chimpanzee study sites (figure 1h and the electronic supplementary material, S1).

Figure 1. (i) Support for the opportunity hypothesis: (a) insectivory tool use by chimpanzees and opportunity for innovation (insect encounter likelihood) at Seringbara (b) tool use in nut cracking and opportunity (nut tree densities) across chimpanzee sites (c) tree hole tool use and opportunity (orangutan density × tree hole density) at two orangutan sites (Ketambe, Suaq) (d) Neesia tool use and opportunity (Neesia population size × N orangutans in Neesia population) across sites (black, Sumatran sites grey, Bornean sites white, Batang Toru, Sumatra) (e) tool-use rate to crack nuts by capuchin monkeys and opportunity (catulè nut availability) at Boa Vista (modified from reference [14]) (f) tool use in nut cracking and opportunity (% time on ground) across capuchin monkey sites. (ii) Lack of support for the necessity hypothesis: (g) tool use in ant dipping (% faeces with ants) in relation to fruit availability index by chimpanzees at Seringbara (h) subsistence tool-use variants and number of dry months across chimpanzee sites (i) tree-hole tool use in relation to % trees with ripe fruit by orangutans at Suaq (j) subsistence tool-use variants and maximum % cambium feeding across orangutan sites (k) tool-use rate to crack nuts in relation to food availability index (fruit, kg per ha) by capuchin monkeys at Boa Vista (l) tool-use rate to crack nuts in relation to food availability index (invertebrate, kg per ha) by capuchin monkeys at Boa Vista.

In orangutans, intersite comparisons also supported the opportunity hypothesis [17]. First, tree-hole tool use was present at Suaq, but absent at Ketambe, consistent with 4.5 times more opportunities for such innovation at Suaq (figure 1c and the electronic supplementary material, S2). Second, orangutans were more likely to use tools to extract Neesia seeds at sites where opportunities for invention were higher (figure 1d and the electronic supplementary material, S2). The necessity hypothesis was not supported [17]. First, at Suaq, insect-extraction tool use was not negatively related to fruit availability (figure 1i and the electronic supplementary material, S2). Second, the number of subsistence tool-use variants across orangutan sites was not correlated with the incidence of extreme food scarcity, as indexed by maximum monthly percentage of time individuals feed on cambium (figure 1j and the electronic supplementary material, S2).

The opportunity hypothesis was also supported in bearded capuchin monkeys at Boa Vista, Brazil [14]. Monthly tool-use rate was correlated with the availability of the most exploited species of palm nuts (catulè nuts, Attalea barreirensis figure 1e and the electronic supplementary material, S3). Moreover, stone tool use was related to degree of terrestriality (i.e. opportunities to encounter nuts and stones), because it has been reported only at sites where individuals spend a considerable amount of time on the ground (figure 1f and the electronic supplementary material, S3 modified from reference [19]). In contrast, the necessity hypothesis was not supported. Tool-use rate was not correlated with availability of fruits and invertebrates (figure 1k,l and the electronic supplementary material, S3).

The conclusion from these studies regarding the ecological influences on feeding tool use in three different taxa is that opportunity, not necessity, is the main driver. We showed that (ecological) opportunities influence occurrence of tool use, and likely the species' cultural repertoires. The resources extracted using tools (nuts, honey, insects) are among the nutritionally richest in primate habitats. Hence, extraction pays off, and not just during times of food scarcity.

3. Future directions

The above-mentioned results do not support the necessity hypothesis. Instead, the results support the opportunity hypothesis: the more exposure a population has to opportunities to invent and practice novel tool use, the more likely the behaviour occurs. We reviewed all the available studies testing the two hypotheses in non-human primates. However, because the number of studies is small, additional testing is needed.

We use these findings to propose a model in which three sets of factors, namely environment, sociality and cognition, influence invention, transmission and retention of material culture (figure 2). First, the environment provides ecological opportunities, in terms of resource density and likelihood to encounter them, which prompt innovation, transmission and retention of tool use. Second, social opportunities for tool use in terms of social tolerance, gregariousness and leftover artefacts from tool-use activities [20] influence transmission and retention of tool use. Third, cognitive capacities for tool use in terms of individual and social learning abilities are also important. In innovation, individual learning plays a crucial role, whereas socially biased learning is essential for transmission of tool use among group members.

Figure 2. The three-factor model of primate material culture (modified from reference [10] by adding ‘environment’ and ‘retention’). White arrows, direct influence black arrows, causal sequence.

The proposed model provides a framework for future research on the emergence and distribution of material culture across primate, as well as non-primate species [21]. It provides a unifying perspective on the emergence of tool use, which may help to explain variation in tool-use diversity and complexity across populations. Lastly, the model allows us to further assess the roles of the environment, sociality and cognition across species with varying social systems and ecological settings.


Footnotes

‡ Present address: Radcliffe Institute for Advanced Study, Harvard University, Cambridge MA 02138, USA.

Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

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Propagation of tool use in primates? - Biology

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Use of Assisted Reproductive Technologies in the Propagation of Rhesus Macaque Offspring

D. P. Wolf, 1,2,* S. Thormahlen, 1,3 C. Ramsey, 1 R. R. Yeoman, 1 J. Fanton, 4 S. Mitalipov 1

1 aDivision of Reproductive Sciences, Oregon National Primate Research Center, Beaverton, Oregon 97006
2 cDepartments of Obstetrics/Gynecology and Physiology and Pharmacology, Oregon Health and Science Uni
3 dNew England Clinic of Reproductive Medicine, Inc. Reading, Massachusetts 01867
4 bDivision of Animal Resources, Oregon National Primate Research Center, Beaverton, Oregon 97006

* Correspondence: Don P. Wolf, Oregon National Primate Research Center, 505 N.W. 185th Ave., Beaverton, OR 97006. FAX: 503 533 2494 [email protected]

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The assisted reproductive technologies (ARTs) as tailored to the production of rhesus monkeys at the Oregon National Primate Research Center (ONPRC) are described. Efficient fertilization of mature oocytes recovered by aspiration from females subjected to follicular stimulation was achieved with fresh or frozen sperm by intracytoplasmic sperm injection (ICSI). Embryo development to the early cleavage stage occurred at high frequency. Cryopreserved embryos showed high postthaw survival and were also transferred in efforts to establish pregnancies. Three methods of transfer were evaluated, two involving embryo placement into the oviduct, laparoscopy and minilaparotomy, and a nonsurgical, transcervical approach that resulted in uterine deposition. Early cleaving embryos (Days 1–4) were transferred into the oviducts of synchronized recipients with optimal results and pregnancy rates of up to 36%. Pregnancy rates were similar when two fresh or frozen embryos were transferred (28– 30%), although more than two embryos had to be thawed to compensate for embryo loss during freeze-thawing. Normal gestational lengths, birth weights, and growth curves were seen with ART-produced infants compared with infants produced by natural mating in the timed mated breeding (TMB) colony at the ONPRC. In 72 singleton pregnancies established following the transfer of ART-produced embryos, the live-birth rate, at 87.5%, was statistically identical to that for the TMB colony. Further development of the ARTs should result in increasing use of these techniques to augment conventional approaches to propagating monkeys, especially those of defined genotypes.

D. P. Wolf , S. Thormahlen , C. Ramsey , R. R. Yeoman , J. Fanton , and S. Mitalipov "Use of Assisted Reproductive Technologies in the Propagation of Rhesus Macaque Offspring," Biology of Reproduction 71(2), 486-493, (1 August 2004). https://doi.org/10.1095/biolreprod.103.025932

Received: 26 November 2003 Accepted: 1 March 2004 Published: 1 August 2004

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CONCLUDING REMARKS

There is now a large body of knowledge regarding in vitro-propagated DC and in vivo DC of OWP species, particularly macaques, and emerging understanding of DC in NWP species. This understanding of DC biology in NHP adds to and complements previous and ongoing work in humans and small animal systems.

NHP DC exist within the paradigm of human DC and may be propagated in vitro or isolated in vivo using protocols well-established for human cells. In particular, in vitro DC propagation in NHP is technically feasible and is capable of generating large numbers of DC for characterization, manipulation, and potential therapeutic use. This understanding of DC biology in NHP is important, as it enables the preclinical testing of DC therapies in models that closely resemble human diseases. However, important differences exist between human and NHP DC and between NHP species, particularly surface molecule expression and some aspects of maturation and function, and these differences need to be considered carefully when designing such translational studies.


FEF inactivation with improved optogenetic methods

Optogenetic methods have been highly effective for suppressing neural activity and modulating behavior in rodents, but effects have been much smaller in primates, which have much larger brains. Here, we present a suite of technologies to use optogenetics effectively in primates and apply these tools to a classic question in oculomotor control. First, we measured light absorption and heat propagation in vivo, optimized the conditions for using the red-light-shifted halorhodopsin Jaws in primates, and developed a large-volume illuminator to maximize light delivery with minimal heating and tissue displacement. Together, these advances allowed for nearly universal neuronal inactivation across more than 10 mm 3 of the cortex. Using these tools, we demonstrated large behavioral changes (i.e., up to several fold increases in error rate) with relatively low light power densities (≤100 mW/mm 2 ) in the frontal eye field (FEF). Pharmacological inactivation studies have shown that the FEF is critical for executing saccades to remembered locations. FEF neurons increase their firing rate during the three epochs of the memory-guided saccade task: visual stimulus presentation, the delay interval, and motor preparation. It is unclear from earlier work, however, whether FEF activity during each epoch is necessary for memory-guided saccade execution. By harnessing the temporal specificity of optogenetics, we found that FEF contributes to memory-guided eye movements during every epoch of the memory-guided saccade task (the visual, delay, and motor periods).

Keywords: FEF Jaws memory-guided saccade optogenetics primate.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Memory-guided saccade task with illumination…

Memory-guided saccade task with illumination (or sham) at one of three task times…

In vivo measurement of visible…

In vivo measurement of visible light propagation. Average light decrease with distance from…

Illuminator broadly distributes light to…

Illuminator broadly distributes light to inhibit a large volume of primate cortex. (…

Nearly universal inactivation of FEF…

Nearly universal inactivation of FEF neurons during the memory-guide saccade task dramatically increases…

Optogenetic inactivation significantly increases error…

Optogenetic inactivation significantly increases error rates and alters saccade metrics. ( A )…


Primates: The Opposable Thumb

The evolution of the opposable or prehensile thumb is usually associated with Homo habilis, the forerunner of Homo sapiens.[2][3][4] This, however, is the suggested result of evolution from Homo erectus (around 1 MYA) via a series of intermediate anthropoid stages, and is therefore a much more complicated link.

The most important factors leading to the habile hand (and its thumb) are:

    the freeing of the hands from their walking requirements - still so crucial for apes today, as they have hands for feet, which in its turn was one of the consequences of the gradual pithecanthropoid and anthropoid adoption of the erect bipedal walking gait

Importance of the opposable thumb

The thumb, unlike other fingers, is opposable, in that it is the only digit on the human hand which is able to oppose or turn back against the other four fingers, and thus enables the hand to refine its grip to hold objects which it would be unable to do otherwise. The opposable thumb has helped the human species develop more accurate fine motor skills. It is also thought to have directly led to the development of tools, not just in humans or their evolutionary ancestors, but other primates as well.[6][7] The thumb, in conjunction with the other fingers make humans and other species with similar hands some of the most dexterous in the world.[8]

Other animals with thumbs

Many animals, primates and others, also have some kind of opposable thumb or toe:

* Bornean Orangutan - opposable thumbs on all four hands. The interdigital grip gives them the ability to pick fruit.
* Gorillas - opposable on all four hands.
* Chimpanzees have opposable thumbs on all four hands.
* Lesser Apes have opposable thumbs on all four hands.
* Old World Monkeys, with some exceptions, such as the genera, Piliocolobus and Colobus.
* Cebids (New World primates of Central and South America) - some have opposable thumbs
* Koala - opposable toe on each foot, plus two opposable digits on each hand
* Opossum - opposable thumb on rear feet
* Giant Panda - Panda paws have five clawed fingers plus an extra bone that works like an opposable thumb. This "thumb" is not really a finger (like the human thumb is), but an extra-long sesamoid bone that works like a thumb.
* Troodon - a birdlike dinosaur with partially opposable thumbs.
* Raccoon - a common mammal with thumbs, which are not opposables.


Abstract

The question of whether any species except humans exhibits culture has generated much debate, partially due to the difficulty of providing conclusive evidence from observational studies in the wild. A starting point for demonstrating the existence of culture that has been used for many species including chimpanzees and orangutans is to show that there is geographic variation in the occurrence of particular behavioral traits inferred to be a result of social learning and not ecological or genetic influences. Gorillas live in a wide variety of habitats across Africa and they exhibit flexibility in diet, behavior, and social structure. Here we apply the ‘method of exclusion’ to look for the presence/absence of behaviors that could be considered potential cultural traits in well-habituated groups from five study sites of the two species of gorillas. Of the 41 behaviors considered, 23 met the criteria of potential cultural traits, of which one was foraging related, nine were environment related, seven involved social interactions, five were gestures, and one was communication related. There was a strong positive correlation between behavioral dissimilarity and geographic distance among gorilla study sites. Roughly half of all variation in potential cultural traits was intraspecific differences (i.e. variability among sites within a species) and the other 50% of potential cultural traits were differences between western and eastern gorillas. Further research is needed to investigate if the occurrence of these traits is influenced by social learning. These findings emphasize the importance of investigating cultural traits in African apes and other species to shed light on the origin of human culture.

Citation: Robbins MM, Ando C, Fawcett KA, Grueter CC, Hedwig D, Iwata Y, et al. (2016) Behavioral Variation in Gorillas: Evidence of Potential Cultural Traits. PLoS ONE 11(9): e0160483. https://doi.org/10.1371/journal.pone.0160483

Editor: Roscoe Stanyon, University of Florence, ITALY

Received: February 7, 2016 Accepted: July 20, 2016 Published: September 7, 2016

Copyright: © 2016 Robbins et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper.

Funding: This work was supported by the Max Planck Society.

Competing interests: The authors have declared that no competing interests exist.


Contents

A transposition in which the transposed material is copied to the transposition site, rather than excised from the original site. [ citation needed ]

Long strands of repetitive DNA can be found at each end of a LTR retrotransposon. These are termed long terminal repeats (LTRs) that are each a few hundred base pairs long, hence retrotransposons with LTRs have the name long terminal repeat (LTR) retrotransposon. LTR retrotransposons are over 5 kilobases long. Between the long terminal repeats there are genes that can be transcribed equivalent to retrovirus genes gag and pol. These genes overlap so they encode a protease that processes the resulting transcript into functional gene products. Gag gene products associate with other retrotransposon transcripts to form virus-like particles. Pol gene products include enzymes reverse transcriptase, integrase and ribonuclease H domains. Reverse transcriptase carries out reverse transcription of retrotransposon DNA. Integrase 'integrates' retrotransposon DNA into eukaryotic genome DNA. Ribonuclease cleaves phosphodiester bonds between RNA nucleotides.

LTR retrotransposons encode transcripts with tRNA binding sites so that they can undergo reverse transcription. The tRNA-bound RNA transcript binds to a genomic RNA sequence. Template strand of retrotransposon DNA can hence be synthesised. Ribonuclease H domains degrade eukaryotic genomic RNA to give adenine- and guanine-rich DNA sequences that flag where the complementary noncoding strand has to be synthesised. Integrase then 'integrates' the retrotransposon into eukaryotic DNA using the hydroxyl group at the start of retrotransposon DNA. This results in a retrotransposon flagged by long terminal repeats at its ends. Because the retrotransposon contains eukaryotic genome information it can insert copies of itself into other genomic locations within a eukaryotic cell.

An endogenous retrovirus is a retrovirus without virus pathogenic effects that has been integrated into the host genome by inserting their inheritable genetic information into cells that can be passed onto the next generation like a retrotransposon. [8] Because of this, they share features with retroviruses and retrotransposons. When the retroviral DNA is integrated into the host genome they evolve into endogenous retroviruses that influence eukaryotic genomes. So many endogenous retroviruses have inserted themselves into eukaryotic genomes that they allow insight into biology between viral-host interactions and the role of retrotransposons in evolution and disease. Many retrotransposons share features with endogenous retroviruses, the property of recognising and fusing with the host genome. However, there is a key difference between retroviruses and retrotransposons, which is indicated by the env gene. Although similar to the gene carrying out the same function in retroviruses, the env gene is used to determine whether the gene is retroviral or retrotransposon. If the gene is retroviral it can evolve from a retrotransposon into a retrovirus. They differ by the order of sequences in pol genes. Env genes are found in LTR retrotransposon types Ty1-copia (Pseudoviridae), Ty3-gypsy (Metaviridae) and BEL/Pao. [9] [8] They encode glycoproteins on the retrovirus envelope needed for entry into the host cell. Retroviruses can move between cells whereas LTR retrotransposons can only move themselves into the genome of the same cell. [10] Many vertebrate genes were formed from retroviruses and LTR retrotransposons. One endogenous retrovirus or LTR retrotransposon has the same function and genomic locations in different species, suggesting their role in evolution. [11]

Like LTR retrotransposons, non-LTR retrotransposons contain genes for reverse transcriptase, RNA-binding protein, nuclease, and sometimes ribonuclease H domain [12] but they lack the long terminal repeats. RNA-binding proteins bind the RNA-transposition intermediate and nucleases are enzymes that break phosphodiester bonds between nucleotides in nucleic acids. Instead of LTRs, non-LTR retrotransposons have short repeats that can have an inverted order of bases next to each other aside from direct repeats found in LTR retrotransposons that is just one sequence of bases repeating itself.

Although they are retrotransposons, they cannot carry out reverse transcription using an RNA transposition intermediate in the same way as LTR retrotransposons. Those two key components of the retrotransposon are still necessary but the way they are incorporated into the chemical reactions is different. This is because unlike LTR retrotransposons, non-LTR retrotransposons do not contain sequences that bind tRNA.

They mostly fall into two types – LINEs and SINEs. SVA elements are the exception between the two as they share similarities with both LINEs and SINEs, containing Alu elements and different numbers of the same repeat. SVAs are shorter than LINEs but longer than SINEs.

While historically viewed as "junk DNA", research suggests in some cases, both LINEs and SINEs were incorporated into novel genes to form new functions. [13]

LINEs Edit

When a LINE is transcribed, the transcript contains an RNA polymerase II promoter that ensures LINEs can be copied into whichever location it inserts itself into. RNA polymerase II is the enzyme that transcribes genes into mRNA transcripts. The ends of LINE transcripts are rich in multiple adenines, [14] the bases that are added at the end of transcription so that LINE transcripts would not be degraded. This transcript is the RNA transposition intermediate.

The RNA transposition intermediate moves from the nucleus into the cytoplasm for translation. This gives the two coding regions of a LINE that in turn binds back to the RNA it is transcribed from. The LINE RNA then moves back into the nucleus to insert into the eukaryotic genome.

LINEs insert themselves into regions of the eukaryotic genome that are rich in bases AT. At AT regions LINE uses its nuclease to cut one strand of the eukaryotic double-stranded DNA. The adenine-rich sequence in LINE transcript base pairs with the cut strand to flag where the LINE will be inserted with hydroxyl groups. Reverse transcriptase recognises these hydroxyl groups to synthesise LINE retrotransposon where the DNA is cut. Like with LTR retrotransposons, this new inserted LINE contains eukaryotic genome information so it can be copied and pasted into other genomic regions easily. The information sequences are longer and more variable than those in LTR retrotransposons.

Most LINE copies have variable length at the start because reverse transcription usually stops before DNA synthesis is complete. In some cases this causes RNA polymerase II promoter to be lost so LINEs cannot transpose further. [15]

Human L1 Edit

LINE-1 (L1) retrotransposons make up a significant portion of the human genome, with an estimated 500,000 copies per genome. Genes encoding for human LINE1 usually have their transcription inhibited by methyl groups binding to its DNA carried out by PIWI proteins and enzymes DNA methyltransferases. L1 retrotransposition can disrupt the nature of genes transcribed by pasting themselves inside or near genes which could in turn lead to human disease. LINE1s can only retrotranspose in some cases to form different chromosome structures contributing to differences in genetics between individuals. [17] There is an estimate of 80–100 active L1s in the reference genome of the Human Genome Project, and an even smaller number of L1s within those active L1s retrotranspose often. L1 insertions have been associated with tumorigenesis by activating cancer-related genes oncogenes and diminishing tumor suppressor genes.

Each human LINE1 contains two regions from which gene products can be encoded. The first coding region contains a leucine zipper protein involved in protein-protein interactions and a protein that binds to the terminus of nucleic acids. The second coding region has a purine/pyrimidine nuclease, reverse transcriptase and protein rich in amino acids cysteines and histidines. The end of the human LINE1, as with other retrotransposons is adenine-rich. [18] [19] [20]

SINEs Edit

SINEs are much shorter (300bp) than LINEs. [21] They share similarity with genes transcribed by RNA polymerase II, the enzyme that transcribes genes into mRNA transcripts, and the initiation sequence of RNA polymerase III, the enzyme that transcribes genes into ribosomal RNA, tRNA and other small RNA molecules. [22] SINEs such as mammalian MIR elements have tRNA gene at the start and adenine-rich at the end like in LINEs.

SINEs do not encode a functional reverse transcriptase protein and rely on other mobile transposons, especially LINEs. [23] SINEs exploit LINE transposition components despite LINE-binding proteins prefer binding to LINE RNA. SINEs cannot transpose by themselves because they cannot encode SINE transcripts. They usually consist of parts derived from tRNA and LINEs. The tRNA portion contains an RNA polymerase III promoter which the same kind of enzyme as RNA polymerase II. This makes sure the LINE copies would be transcribed into RNA for further transposition. The LINE component remains so LINE-binding proteins can recognise the LINE part of the SINE.

Alu elements Edit

Alus are the most common SINE in primates. They are approximately 350 base pairs long, do not encode proteins and can be recognized by the restriction enzyme AluI (hence the name). Their distribution may be important in some genetic diseases and cancers. Copy and pasting Alu RNA requires the Alu's adenine-rich end and the rest of the sequence bound to a signal. The signal-bound Alu can then associate with ribosomes. LINE RNA associates on the same ribosomes as the Alu. Binding to the same ribosome allows Alus of SINEs to interact with LINE. This simultaneous translation of Alu element and LINE allows SINE copy and pasting.

SVA elements are present at lower levels than SINES and LINEs in humans. The starts of SVA and Alu elements are similar, followed by repeats and an end similar to endogenous retrovirus. LINEs bind to sites flanking SVA elements to transpose them. SVA are one of the youngest transposons in great apes genome and among the most active and polymorphic in the human population.

A recent study developed a network method that reveals SVA retroelement (RE) proliferation dynamics in hominid genomes. [24] The method enable to track the course of SVA proliferation, identify yet unknown active communities, and detect tentative "master REs" that play key roles in SVA propagation. Thus, providing support for the fundamental "master gene" model of RE proliferation.

Retrotransposons ensure they are not lost by chance by occurring only in cell genetics that can be passed on from one generation to the next from parent gametes. However, LINEs can transpose into the human embryo cells that eventually develop into the nervous system, raising the question whether this LINE retrotransposition affects brain function. LINE retrotransposition is also a feature of several cancers, but it is unclear whether retrotransposition itself causes cancer instead of just a symptom. Uncontrolled retrotransposition is bad for both the host organism and retrotransposons themselves so they have to be regulated. Retrotransposons are regulated by RNA interference. RNA interference is carried out by a bunch of short non-coding RNAs. The short non-coding RNA interacts with protein Argonaute to degrade retrotransposon transcripts and change their DNA histone structure to reduce their transcription.

LTR retrotransposons came about later than non-LTR retrotransposons, possibly from an ancestral non-LTR retrotransposon acquiring an integrase from a DNA transposon. Retroviruses gained additional properties to their virus envelopes by taking the relevant genes from other viruses using the power of LTR retrotransposon.

Due to their retrotransposition mechanism, retrotransposons amplify in number quickly, composing 40% of the human genome. The insertion rates for LINE1, Alu and SVA elements are 1/200 – 1/20, 1/20 and 1/900 respectively. The LINE1 insertion rates have varied a lot over the past 35 million years, so they indicate points in genome evolution.

Notably a large number of 100 kilobases in the maize genome show variety due to the presence or absence of retrotransposons. However since maize is unusually genetically compared to other plants it cannot be used to predict retrotransposition in other plants.



Comments:

  1. Escorant

    This can and should be discussed :) endlessly



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