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The Role of Transposable Elements in Speciation

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The Role of Transposable Elements in Speciation G C A T T A C G G C A T genes Review The Role of Transposable Elements in Speciation Antonio Serrato-Capuchina and Daniel R. Matute * Biology Department, Genome Sciences Building, University of North Carolina, Chapel Hill, NC 27514, USA; [email protected] * Correspondence: [email protected] Received: 30 January 2018; Accepted: 26 April 2018; Published: 15 May 2018 Abstract: Understanding the phenotypic and molecular mechanisms that contribute to genetic diversity between and within species is fundamental in studying the evolution of species. In particular, identifying the interspecific differences that lead to the reduction or even cessation of gene flow between nascent species is one of the main goals of speciation genetic research. Transposable elements (TEs) are DNA sequences with the ability to move within genomes. TEs are ubiquitous throughout eukaryotic genomes and have been shown to alter regulatory networks, gene expression, and to rearrange genomes as a result of their transposition. However, no systematic effort has evaluated the role of TEs in speciation. We compiled the evidence for TEs as potential causes of reproductive isolation across a diversity of taxa. We find that TEs are often associated with hybrid defects that might preclude the fusion between species, but that the involvement of TEs in other barriers to gene flow different from postzygotic isolation is still relatively unknown. Finally, we list a series of guides and research avenues to disentangle the effects of TEs on the origin of new species. Keywords: speciation; transposable elements; reproductive isolation 1. Introduction Speciation is the evolutionary process by which one lineage splits into two reproductively isolated groups of organisms [1]. One of the central goals of speciation research is to understand the processes that drive the evolution of reproductive isolation (RI) between species [2–6]. Significant strides have been made towards identifying barriers that generate RI between species [1,7], the processes underlying their evolution [2,3,8–11], and the rate at which they evolve during speciation [4,5,12–15]. Even though some progress has been made in identifying genes and loci associated with RI, few studies have explored the evolutionary processes that produced these barriers. Because of this, there is not yet a consensus as to what types of mutations or which mechanisms are typically involved in speciation or RI. There are two broad approaches to identify the genetic underpinnings of RI. First, if crosses can be made, one can genetically map the loci underlying RI between organisms. Such studies can establish the genetic changes that maintain species identity and, if divergence is recent, potentially reveal the molecular changes that were initially involved in speciation. This approach is particularly informative when coupled with closely related organisms at different stages of reduced gene exchange [1,16,17]. An alternative approach is to assess whether a particular type of molecular change is commonly associated with isolation between genotypes. If a barrier to gene flow is commonly caused by a certain type of molecular change, then one can argue that that molecular change is important in either the origin of new species or the persistence of them when they face the possibility of collapse through gene flow. This approach has, for example, revealed that chromosomal inversions are commonly associated with the suppression of recombination and frequently harbor gene combinations involved in isolation between species [18,19] (reviewed in [20]). However, this approach has rarely been used to understand Genes 2018, 9, 254; doi:10.3390/genes9050254 www.mdpi.com/journal/genes Genes 2018, 9, x FOR PEER REVIEW 2 of 28 Genes 2018, 9, 254 2 of 29 approach has rarely been used to understand the impact of other molecular changes on RI. Here we thehighlight impact transposable of other molecular elements changes as recurring on RI. Hereagents we that highlight underlie transposable a variety of elements manifestations as recurring of RI, agentswhich thatsuggests underlie they a varietyshould ofbe manifestationsexplored across of RI,various which taxa suggests in order they to should better be understand explored across their variousmechanistic taxa and in order evolutionary to better understandcontributions. their mechanistic and evolutionary contributions. Transposable elementselements (TEs)(TEs) areare DNADNA sequencessequences ableable to copy and insert themselves throughout the genome.genome. TEs TEs represent represent up up to to 80% 80% of nuclear DNA in plants, 3–20% in fungi,fungi, and 3–52%3–52% inin metazoans [[21–23].21–23]. TEs TEs are classified classified according to the mechanismmechanism theythey useuse toto transpose.transpose. Class I elements require anan RNARNA intermediateintermediate inin orderorder toto integrate/duplicateintegrate/duplicate themselves within a genome, whilewhile ClassClass II II elements elements act act without without an intermediate an intermed throughiate through a cut-and-paste a cut-and-paste mechanism mechanism that replicates that itsreplicates DNA directly its DNA to directly DNA as to it DNA mobilizes as it mobilizes (Figure1). (Figure A full classification1). A full classification of TEs is of shown TEs is in shown Table1 in. Interestingly,Table 1. Interestingly, the predominant the predominant class ofclass TEs of canTEs can vary vary greatly greatly between between taxa taxa [24 [24–28]–28] andand species, and theirtheir genomicgenomic frequency, frequency, location, location, and and activity activity levels levels can can vary vary greatly greatly even even at the at population the population level. TEslevel. were TEs describedwere described for the for first the time first intime maize in maiz by Barbarae by Barbara McClintock McClintock in 1950 in [195029] where[29] where they leadthey tolead somatic to somatic mutations mutations affecting affecting various various phenotypes/genes phenotypes/genes depending depending on their on chromosomal their chromosomal location andlocation transposition and transposition time. The time. insertion The insertion of a TE can of a disrupt TE can the disrupt coding the or coding regulatory or regulatory sequences sequences of genes, whichof genes, can which cause can deleterious cause deleterious effects by theeffects modifying by the modifying or eliminating or eliminating a gene’s expression a gene’s [expression30–34]. TEs [30– are ubiquitous34]. TEs are throughoutubiquitous naturethroughout [35–37 nature] and [35–37] their effect and ontheir their effect hosts’ on fitnesstheir hosts’ is generally fitness is considered generally toconsidered be deleterious; to be TEs deleterious; are commonly TEs consideredare commonl selfishy considered elements. However,selfish elements. gene disruptions However, are gene not thedisruptions only consequence are not the of only TEs asconsequence they transpose of TEs throughout as they transpose the genome. throughout TEs can alsothe genome. cause regulatory TEs can changes,also cause genomic regulatory expansions, changes, and genomic generate expans new chromosomalions, and generate variants new through chromosomal the generation variants of inversions.through the Moreover, generation TEs of inversions. can produce Moreover, all of these TE changess can produce rapidly all [38 of– these40] and changes in response rapidly to [38–40] abiotic stressors—aand in response hypothesis to abiotic first stressors—a advanced hypothesis by McClintock first [advanced29]. These by changes McClintock can provide [29]. These genetic changes and phenotypiccan provide novelties genetic and upon phenotypic which selection novelties can actupon [41 ,42which]. Due selection to their can potential act [41,42]. to generate Due noveltyto their whenpotential it is to needed, generate some novelty have when hypothesized it is needed, that so TEsme are have maintained hypothesized in genomes that TEs through are maintained multilevel in selectiongenomes [through43–45]. multilevel selection [43–45]. CLASS 1 – RETROTRANSPOSONS CLASS 2 – DNA TRANSPOSONS Types Types 5’ 3’ 5’ 3’ LTR LTR GAG POL LTR TIR TIR Transposase TIR Helitron LINE GAG POL PolyA Replicase Helicase SINE Left monomer A-rich Right monomer PolyA Maverick Integrase Polymerase Copy and Paste mechanism Cut and Paste mechanism 5’ 3’ 5’ 1 HOST DNA 3’ Transcription Excision RNA INTERMEDIARY DNA INTERMEDIARY Integration Reverse transcription 5’ 3’ Former 2 site DNA INTERMEDIARY Host DNA Integration Transposable element 1 2 5’ 3’ GAG gag gene, encodes structural proteins POL pol gene, encodes for a cleaving protease, reverse transcriptase and integrase TIR Terminal inverted repeats Figure 1.1.A A graphical graphical classification classification of transposable of transposable elements el (TEs).ements The (TEs). left panel The shows left Classpanel 1 retrotransposons,shows Class 1 andretrotransposons, the right panel and shows the right Class panel 2 DNA shows transposons. Class 2 DNA The transposons. upper panels The show upper three panels examples show of three the geneticexamples structure of the ofgenetic each ofstructure these two of classeseach of of these elements. two classes The lower of elements. panels show The thelower mode panels of movement show the (transpositionmode of movement mechanism) (transposition of each class. mechanism)LTR: Long Terminal of each class. Repeats; LTRLINE: Long: Long Terminal interspersed Repeats; nuclear LINE elements;: Long SINEinterspersed:
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