Hybrid Genome Evolution by Transposition: An Update · 2019. 2. 13. · hybrids almost exclusively...

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Journal of Heredity, 2019, 124–136doi:10.1093/jhered/esy040

Original ArticleAdvance Access publication September 8, 2018

Special Issue Article

Hybrid Genome Evolution by Transposition: An UpdateAntonio Fontdevila

From the Grup de Genòmica, Bioinformàtica i Biologia Evolutiva, Departament de Genètica i Microbiologia, Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès, Bellaterra, Spain.

Address correspondence to A. Fontdevila at the address above, or e-mail: [email protected].

Received May 21, 2018; First decision June 30, 2018; Accepted August 6, 2018.

Corresponding Editor: Therese Markow

Abstract

Contrary to the view that hybrids are lineages devoid of evolutionary value, a number of case studies that have been lately reported show how hybrids are at the origin of many species. Some well-documented cases demonstrate that bursts of transposition often follow hybridization, generating new genetic variability. Studies in hybrid transposition strongly suggest that epigenetic changes and divergence in piRNA pathways drive deregulation in TE landscapes. Here, I have focused on mechanisms acting in Drosophila hybrids between two cactophilic species. The results reported here show that while hybrid instability by transposition is a genome-wide event, deregulation by TE overexpression in hybrid ovaries is not a general rule. When piRNA pools of ovaries are studied, results show that TEs with parental differences higher than 2-fold in their piRNA amounts are not more commonly deregulated in hybrids than TEs with similar levels, partially discrediting the generality of the maternal cytotype hypothesis. Some promising results on the piRNA pathway global failure hypothesis, which states that accumulated divergence of piRNA effector proteins is responsible for hybrid TE deregulation, have also been obtained. Altogether, these results suggest that TE deregulation might be driven by several interacting mechanisms. A natural scenario is proposed in which genome instability by transposition leads to hybrid genome reorganization. Small hybrid populations, subjected to natural selection helped by genetic drift, evolve new adaptations adapted to novel environments. The final step is either introgression or even a new hybrid species.

Subject areas: Gene action, regulation and transmission, Molecular adaptation and selectionKeywords: Drosophila hybrids, genetic instability, misregulation, piRNA, speciation, Transposable elements

There is little doubt that genomes of some if not all organ-

isms are fragile and that drastic changes may occur at

rapid rates. These can lead to new genomic organizations

and modified controls of type and time of gene expres-

sion. It is reasonable to believe that such genome shocks

are responsible for the release of otherwise silent ele-

ments… Since the types of genome restructuring induced

by such elements know few limits, their extensive release,

followed by stabilization, could give rise to new species or

even new genera.

McClintock (1980)

The role of hybridization in evolution: an introduction

Hybrids were often considered dead ends, devoid of evolutionary significance, by early neodarwinian evolutionists, who associated

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hybrids almost exclusively to hybrid incompatibility as a definition of the biological species (Dobzhansky 1937). Yet, new evidence sup-ports them as drivers of species evolution (Arnold 1997; Fontdevila 2011). In particular, alloploid speciation, discovered about one cen-tury ago, has been recognized as a common hybrid speciation in plants ever since, but natural hybrid speciation without duplication of hybrid genomes (homoploid speciation), longtime disregarded as rare or inexistent, is now widely documented through experimen-tal reticulate phylogenies and extensive genomic studies in plants, animals, and fungi (Rieseberg and Noyes 1998; Greig et al. 2002; Arnold 2006; Mallet 2007; Abbott et al. 2013; Leducq et al. 2016). Besides speciation, outcomes of natural hybridization include merg-ing of genomes, reinforcement of prezygotic isolation and intro-gression (Abbott et al. 2013). Botanists were early favoring hybrid speciation due to their observations in nature, in particular, the ubiq-uity of natural plant hybridization (Mallet 2005), and did not much agree with the universal definition of the biological species concept. Recently, many cases of plant hybrid speciation have been studied in their ecology and genetics, such as in Iris nelsonii and Helianthus anomalus (Gross and Rieseberg 2005; Arnold 2006). Animal hybrid species were more difficult to detect by zoologists, who became skep-tic to hybrid speciation and sponsored the hybrid incompatibility as the biological criteria for species concept. With new advances in gene and genome technology, however, many cases of hybrid homoploid speciation are being described in animals, vertebrates and inverte-brates alike (Arnold 2006; see Fontdevila 2011, table 4.2, p. 134). Recently, research on fungi have revealed that budding yeasts can also evolve by homoploid speciation, such as in natural populations of Saccharomyces paradoxus (Leducq et al. 2016).

Hybridization (polyploid and homoploid) is commonly followed by genome reorganization (Rieseberg et al. 1996; Michalak 2009; Garcia Guerreiro 2014; see for a review Fontdevila 2011). This is observed not only in ancient hybrids, but also in experimentally pro-duced synthetic hybrids. For example, the genus Brassica, an ances-tral hexaploid, has undergone extensive karyotipic rearrangements since polyploidization (Lagerkrantz and Lydiate 1996). Similar reor-ganizations occur in homoploid hybrid species such as in Helianthus anomalus, a hybrid species originated by hybridization between H. annus and H. petiolaris. Rieseberg et al. (1996) have mimicked this natural hybridization in the laboratory, obtaining, after 5 gen-erations of selfing and/or backcrossing, 3 fertile, synthetic hybrid lineages that showed a high concordance in genomic composition using 197 RAPD markers. Most surprisingly, this repatterned gen-ome was concordant with that of H. anomalus, the natural hybrid species, suggesting that natural genomic reorganization is not only rapid but also repeatable.

Causes of hybrid genome reorganization and their subsequent evolutionary importance have been the focus of much research in recent decades. The building of a natural scenario to bolster the role of hybridization in evolution has also captured the interest of evo-lutionists. Here, I will update both interests mainly focusing on the putative evolutionary role of transposition by transposable elements.

Contribution of transposable elements (TEs) to genome evolution

Now we know that many gene mutations are the result of TE insertions, which can amount to more than 80% in Drosophila (Ashburner 1989) and about 10% in mice (Platt et al. 2018) of point mutations. Though these mutations are often deleterious, a signifi-cant proportion of these insertions generate novel patterns of gene

expression of utmost importance for evolution. Ever since the begin-ning of TE research, the number of cases benefiting host evolution has increasingly been reported (Biémont and Vieira 2006). TE-related new functions include changes in regulatory functions, origin of new exons (exonization), host cell repair, exon shuffling, new functions of heterochromatic TE clusters, and promotion of recombination, allowing for restructuring of the genome whose impact exceeds that of point mutations (Kidwell and Lisch 1997; Kumar and Bennetzen 1999; Platt et al. 2018).

TEs also contribute to genome size. In humans, L1 is responsible for about one fourth of human genome and Alu and processed pseu-dogenes amount 10% of its genome; in fact almost 50% of the human genome is occupied by TEs; in Drosophila TEs make up 10–15% of the genome; more than 50 % of the maize genome originates from TEs, and Ty1-copia makes up more than 40 % of the genome in many plants (Biémont and Vieira 2005; Kidwell 2005; Ungerer et al. 2006; Platt et al. 2018). TEs are also drivers of genome rearrange-ments throughout ectopic recombination, generating duplications, deletions, and inversions, for example, in yeast (Dunn et al. 2013) and Drosophila (Delprat et al. 2009), and also due to transposition of genes or part of genes which are amplified and dispersed linked to adjacent TEs, for instance, MULE in plants like maize, Arabidopsis, and rice (Wessler 2006), SVA in hominids (Cordaux and Batzer 2009), and L1 in cultured human cells (Moran et al. 1999).

All this evidence has been related to some environmental and genomic shocks occasionally experienced by organisms. Among the latter, hybridization has attracted the most interest to evolutionists in view of the increasing importance of hybrids as drivers of speci-ation and evolution in general. Here, I will sketch an update of this historically contentious topic.

Early evidence of co-ocurrence of hybridization and transposition

Sturtevant (1939) reported, as far as I know, the best early docu-mented case of mutation increase in hybrids. Crossing 2, so called, “races” of Drosophila pseudoobscura, later recognized as 2 differ-ent species (D. pseudoobscura and D. persimilis), he observed, in backcrosses, mutation frequencies 2 orders of magnitude higher than normal spontaneous mutation rates ever recorded. Later, increases in rates of chromosomal rearrangements in hybrids were reported in Nicotiana species, and Caledia and Chironomus subspecies (see references in Labrador and Fontdevila 1994). All these observations were qualified as episodes of genetic instability and their relation-ship to hybridization was not clear until some observations relating TE transposition and hybrids were reported in Chironomus hybrids (Schmidt 1984) and Drosophila (see references in Fontdevila 1992). However, evidence of enhanced transposition in these experiments was indirect, based, mainly, on observed reverse mutations due to TE excision.

The first direct observation of increased transposition in species hybrids, using chromosomal in situ hybridization techniques, was reported by Labrador and Fontdevila (1994) in hybrids between Drosophila buzzatii and D. koepferae, 2 sibling species of the Drosophila repleta group that coexist in the arid zones of Bolivia and NW Argentina. Under experimental conditions they produce F1 hybrid progeny consisting of sterile males and fertile females. These females can be backcrossed to D. buzzatti males and their female progeny sequentially backcrossed to D. buzzatii males during several generations. After a few backcrosses, this procedure allows us to obtain a collection of individuals with a D. buzzatii genome

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introgressed with genomic portions of D. koepferae (introgressed hybrids). Naveira and Fontdevila (1985) observed that progenies of some introgressed hybrids displayed an excess of new chromo-somal rearrangements that could be qualified as an episode of gen-etic instability mediated by interspecific hybridization. This burst of new rearrangements was similar to that previously observed with Nicotiana, Caledia, and Chironomus. Thus, the relationship found between TE transposition and production of new rearrangements in Chironomus hybrids suggested that transposition could also be induced by the buzzatii/koepferae hybridization. This prediction was tested by Labrador et al. (1999) using Osvaldo, a retrotransposon isolated from D. buzzatii (Pantazidis et al. 1999). The screening of new insertions by in situ hybridization was performed in the sec-ond backcross progeny and showed that transposition rates are one order of magnitude higher in introgressed hybrids (1.5–3.9 × 10–2 per element per generation) than in parental D. buzzatii (8.5 × 10–3). These results confirmed those previously obtained by Labrador and Fontdevila (1994). However, in that experiment the use of an inbred D. buzzatii stock and a small sample size impeded the authors from making strong conclusions. On the other hand, both, quantitative treatment of transposition rates and direct observation of trans-position in the experiment of Labrador et al. (1999) led to the firm conclusion that hybrids are triggers of genetic instability by trans-position in Drosophila.

Genome-wide genetic instability by transposition in hybrids

Although the direct relationship between genetic instability and trans-position of Osvaldo was a landmark in the role of hybrids it remained to be seen whether TE mobilization is a universal response to hybrid-ization for all genomic TEs or, on the contrary, it depends on the kind of element. Vela et al. (2014) undertook a genome-wide dissection of TE mobilization in Drosophila interspecific hybrids using AFLP markers, including a quantitative estimation of transposition rates of some TEs, to test the ubiquity of the TE-mediated hybrid instability. Figure 1 shows an example of AFLP gel bands of parental species and hybrids, depicting by arrows those bands specific of hybrids, named as instability markers hereafter. The number of instability markers segregating in hybrids of first (BC1), second (BC2), and third (BC3) backcrosses was 30, 17, and 25, respectively. The number of trans-position markers, those which showed homology with TEs, was 5, 5, and 13 in BC1, BC2, and BC3, respectively (Figure 2), whereas only one was found in the paternal species (D. buzzatii). Thus, the percent-age of genomic instability due to transposition was 16.6%, 29.4%, and 52.0% in BC1, BC2, and BC3, respectively. The remaining frac-tion of instability probably originated by the suppression of a restric-tion site and/or by double-strand breaks that are usually associated to the loss of chromosomal segments or the rearrangement of genetic material (Salomon and Puchta 1998).

Figure 1. Interspecific cross and backcrosses used in experiments. Selective PCR AFLP band patterns. Arrows pointing to gel bands indicate 2 instability markers detected in hybrids from backcross 1 as an example. MWM, molecular weight marker; Dk, D. koepferae; Db, D. buzzatii; HF1, F1 hybrids; BC1, backcross 1. From Vela et al. (2014) doi: 10.1371/journal.pone.0088992g001, reproduced under the Creative Commons Attribution 4.0 International License (CC BY 4.0).

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The transposon display technique employed to estimate trans-position rates has the advantage of amplifying both euchromatic and heterochromatic copies, whereas in situ hybridization, in spite of having been traditionally used to estimate total transposition rates in Drosophila (Labrador and Fontdevila 1994; Vieira and Biémont 1996), only allows to discern euchromatic copies. Thus, transposon display allowed Vela et al. (2014) to compute real trans-position rates of Osvaldo, Helena, and Galileo in hybrid progenies and parental species. They found an overall increase of transpos-ition rate in backcrossed hybrids, but some differences were also detected among progeny families, hybrid crosses, and TEs. Thus, the basal transposition rate of Osvaldo estimated for D.buzzatii and D. koepferae ranged from 0 to 7.2 × 10–4 and it increased by one order of magnitude (10–2 to 10–3) in all backcrosses but one (Supplementary Table 1). When progenies of crosses (hybrid families) were compared for numbers of new insertions (Table 1) significant differences were detected in BC1 and BC3, showing that the effect of hybridization on Osvaldo TE instability depends on the analyzed hybrid families in some backcrosses. Statistical anal-yses (Table 2) also showed significant differences (P < 10–3) for Osvaldo number of insertions between hybrids and parental spe-cies in the 3 backcrosses. In the case of Helena and in spite of

more new insertions detected in hybrids compared with parental species (Supplementary Table 1), differences were not significant (Table 2). For the Galileo element, significant differences between hybrids and parental new insertion numbers were also found in BC1 and BC2 (Table 2). While the basal transposition rate of this element is 0 for parental species, it shows high transposition activ-ity in 2 families of BC1 (1.4 × 10–2), later decreasing in BC2 and BC3 (Supplementary Table 1). Again, when hybrid families are compared (Table 1), they reveal highly significant differences in number of new insertions among them in BC1 and BC2. In sum, while there is a significant overall effect of hybridization on TE instability, these results support, however, the idea that bursts of transposition occur neither equally in all hybrid families, nor with the same intensity for all TEs.

This study constitutes the first genome-wide survey of hybrid instability showing that a high proportion of the instability markers detected in hybrids correspond to TEs. Thus, an average of 32 % of the instability markers detected in the 3 backcross generations corresponds to a wide variety of TEs. The high intensity variabil-ity of instability processes among TEs, and also among backcrosses, however, suggests that many control factors must be considered to understand the role of TEs in hybrid instability. Differences among hybrid families are also unsurprising considering that, despite the introgressed amount of D.koepferae genome is about equal in fami-lies of the same backcross generation, the introgressed genomic regions are different in each family. It is long known that the mobil-ity of TEs is controlled by specific genomic loci; for example, gypsy, Idefix, and Zam are controlled by the locus flamenco (Pelisson et al. 1994; Desset et al. 2003) and P elements by a subtelomeric region of X chromosome (Stuart et al. 2002). These loci comprise fragmented and imperfect copies of retrotransposons that are the precursors of Piwi-interacting RNAs (piRNA) responsible of transcriptional and post-transcriptional TE control (see figure 7 in Brennecke et al. 2007; Rozhkov et al. 2013). Accordingly, Vela et al. (2014) hypoth-esized that TE activation in hybrids could occur in a similar way to that in dysgenic crosses, namely due to the lack of specific maternal piRNAs (the maternal cytotype failure hypothesis: see Picard 1976; Kidwell et al. 1977). Another hypothesis, not exclusive, could be the divergence of genes involved in the piRNA pathway.

Changes in TE expression after interspecific hybridization

Following the same cross scheme, Romero-Soriano et al. (2017) sequenced the ovarian transcriptomes of parental species, D. buz-zatii and D. koepferae, F1 hybrids and backcross BC1, and also the testicular transcriptomes of D.buzzatii and F1. They found that ovaries show significantly higher TE expresssion rate than testes

Table 1. Comparison of the number of new insertions between hybrid families by Kruskal–Wallis test

BC1 BC2 BC3

TEs N χ2 P value χ2 P value χ2 P value

Osvaldo 4 31.18 <10–3** 6.206 0.102 10.877 0.012*Helena 4 4.667 0.198 8.911 0.031* 1.108 0.775Galileo 4 10.768 0.013* 17.623 0.001** 6.875 0.076

TEs: Transposable elements; N: number of families, U: statistic value.*P ≤ 0.05; **P ≤ 0.01; BC1, BC2, and BC3 correspond to backcrosses 1, 2, and 3, respectively.From Vela et al. (2014) doi: 10.1371/journal.pone.0088992g001, reproduced under the Creative Commons Attribution 4.0 International License (CC BY 4.0).

Figure 2. Number of instability markers in hybrids. Instability markers by transposition are depicted in black; those by other origin in gray. Redrawn from Vela et al. (2014) doi: 10.1371/journal.pone.0088992g002, reproduced under the Creative Commons Attribution 4.0 International License (CC BY 4.0).


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(Figure 3A), but no significant differences between parental species and hybrids were detected. Although retrotransposons always show the highest expression category (LINEs followed by LTRs), there are notable differences in TE expression profiles between parentals and hybrids: LTR proportion is increased in hybrid testes and ovaries, and also RC (Helitron) in F1 testes (Figure 3B).

Figure 4 depicts TE expression analyses in hybrid ovaries com-pared with both parental species. It shows 37 TE families signifi-cantly overexpressed in F1 and only 27 in BC1, Gypsy elements exhibiting the highest fold change (FC) values. Unexpectedly, 26 TE families in F1 and 17 in BC1 are unexpressed, though their FC values tend to be lower than those of overexpressed TE families. In general, the global amount of TE deregulation and the FC values are

often lower in BC1 than in F1. Only 21% of deregulated TE families exhibit differences of expression higher than 2-fold between parental species (16 TE families: 14 overexpressed and 2 underexpressed).

In conclusion, this prevalence of ovarian hybrid TE overexpres-sion in deregulation agrees with studies where higher transcription levels in hybrids were reported (Kawakami et al. 2011; Kelleher et al. 2012; Carnelossi et al. 2014; Dion-Côté et al. 2014; García Guerreiro 2015). A few genome-wide surveys, however, reported cases of TEs underexpression in hybrids, but these results were generally poorly discussed. For instance, in lake white fish hybrids (Coregonus sp.), approximately one third (range 29–37%) of differentially expressed TEs are underexpressed (Dion-Côté et al. 2014), and in hybrid sun-flowers (genus Helianthus), F1 hybrids present lower expression in

Table 2. Comparison of the number of new insertions between hybrids and parental species by Mann–Whitney test

Parentals BC1 BC2 BC3

TEs N N U P value N U P value N U P value

Osvaldo 53 16 206.5 <10–3** 65 1170.5 <10–3** 119 1330.5 <10–3**Helena 47 17 372 0.439 65 1440 0.420 127 2772 0.278Galileo 53 17 185 <10–3** 60 1431 0.031* 126 3180 0.107

TEs: transposable elements, N: number of individuals, U: statistic value.*P ≤ 0.05, **P ≤ 0.01; BC1, BC2, and BC3 correspond to backcrosses 1, 2, and 3, respectively. From Vela et al. (2014) doi: 10.1371/journal.

pone.0088992g001, reproduced under the Creative Commons Attribution 4.0 International License (CC BY 4.0).

Figure 3. Transposable element expression summary in D. buzzatii (Dbu), D. koepferae (Dko), F1, and first backcross (BC1). (A) Mean proportion of reads aligning to the TE library. Bars represent standard deviation between replicates. **Wilcoxon’s W = 2, P = 0.016. (B) TE expression profiles following Repbase classification (Jurka et al. 2005): LTR and LINE (class I), DNA and RC/Helitron (class II), Unknown (unclassified). LTR, elements with long terminal repeats; LINE, long interspersed nuclear element; RC, rolling circle elements (or Helitrons). From Romero-Soriano et al. (2017) doi: 10.1093/gbe/evx091, reproduced under the Creative Commons Attribution Non-Commercial 3.0 Unported License (CC BY-NC 3.0).


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the majority of TEs compared with parental species (Renaut et al. 2014). The simultaneous presence of both overexpressed and under-expressed TEs suggests that hybrid TE deregulation underlies a com-mon phenomenon in the genomic shock fueled by hybridization which encompasses the conflict between hybrid short term genome incompatibility and long term evolutionary value of new variability by hybrid transposition. Overexpresion in deregulated TEs, however, is not universal and may be idiosyncratic of parental species and TE families. In sum, the present evidence suggests that causal mecha-nisms of TE deregulation are more complex than expected.

Differences in piRNA pools between parental species ovaries can underlie TE deregulation (Brennecke et al. 2008; Chambeyron et al. 2008), especially when, under the maternal cytotype failure hypoth-esis piRNA levels are lower in the maternal species. Nevertheless, in D.buzzatii-D.koepferae hybrids TEs having lower levels of piRNAs in the maternal species (such as Howilli1 in Figure 6) are not always overexpressed, either in F1 or BC1 (Figure 5i). Reciprocally, TEs having higher levels of piRNAs in the maternal species (such as Gypsy 6-I in Figure 6) are not always underex-pressed in hybrids (Figure 5iii). Hence, differences between piRNA pools following lower levels in the maternal species may account only for some specific cases of TE overexpression (such as TART B1 in Figure 6). Moreover, TEs with parental differences higher than 2-fold (FC) in their piRNA amounts are not more commonly deregulated than families with similar levels (Figure 6). Therefore, the observed pattern of TE deregulation does not always seem to bolster the maternal cytotype failure hypothesis. In view of these results, Romero-Soriano et al. (2017) concluded that they might be explained by the piRNA pathway global failure hypothesis, which

states that divergence of piRNA pathway effector proteins underlies hybrid TE deregulation.

Divergence in piRNA pathway proteins contributes to hybrid instability

The piRNA (Piwi-interacting RNA) pathway (Klattenhoff and Theurkauf 2008; Brennecke and Senti 2010; Tóth et al. 2016) initially produces long piRNA precursors that are cleaved to produce primary piRNAs (Brennecke et al. 2007). Cleavage and subsequent processing of expressed transposon RNAs give rise to additional piRNAs that fuel additional rounds of this transposon defense cycle, which is named the “ping-pong” amplification cycle, giving rise to secondary piRNAs (Brennecke et al. 2007; Gunawardane et al. 2007). A third kind of piR-NAs is produced by phased cleavage of piRNA cluster transcript rem-nants that have first been processed during secondary piRNA biogenesis (Han et al. 2015; Mohn et al. 2015). All transposon-derived piRNAs direct PIWI (P-element induced wimpy testes) proteins (effector proteins) to cleave active transposon transcripts in Drosophila (Brennecke et al. 2007) and works as an effective transposon defense system (Tóth et al. 2016).

Some of the piRNA pathway effector proteins are encoded by genes bearing marks of positive selection (Simkin et al. 2013; Palmer et al. 2018) and divergence between them is likely to account for the TE silencing failure in hybrids (Kelleher et al. 2012). Romero-Soriano et al. (2017) assessed the distribution of identity percentages between D. buzzatii and D. koepferae with a resulting median identity of 97.2% (Figure 7). Then they identified in D. buz-zatii and D. koepferae 30 protein-coding genes known to play a

Figure 4. Ovarian expression of TE families in D. koepferae versus D. buzzatii. Deregulated TE families in hybrids compared with both parental species are depicted in black (underexpressed) and in dark gray (overexpressed). No deregulated TEs are depicted in light gray. Dotted lines represent 2-fold changes between parental expression and the solid line represents the same amount of expression between Dbu and Dko. Names of those TE families with differences of expression higher than 2-fold between parental species are indicated. From Romero-Soriano et al. (2017) doi: 10.1093/gbe/evx091, reproduced under the Creative Commons Attribution Non-Commercial 3.0 Unported License (CC BY-NC 3.0).


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role in TE regulation (Yang and Pillai 2014). Alignments between parental species exhibit identity percentages lower than the median for all but one of all these genes (Figure 7) and some effector pro-teins involved in both piRNA biogenesis (e.g., zucchini, tejas) and TE silencing (e.g., panoramix, maelstrom, Hen1, and qin) were

found among the most divergent proteins (identity <90%). These 30 protein-coding genes also revealed significant expression differ-ences between parental species for all but 3 of them. Interestingly, the 2 main acting genes in secondary piRNA biogenesis, Aubergine (Aub) and Argonaute3 (Ago3) and the krimper gene, involved in the

Figure 6. Parental piRNA populations and TE deregulation in ovaries. Expression of TE-associated piRNA populations in D. koepferae (Dko) versus D. buzzatii (Dbu). Dot lines represent 2-fold changes between parental piRNA amounts and the solid line represents the same piRNA levels between Dbu and Dko. Underlined TE names are examples of families that may be deregulated due to the maternal cytotype hypothesis: underexpressed with more piRNAs in D. koepferae (depicted in black), overexpressed with more piRNAs in D. buzzatii (depicted in dark shade). Names of deregulated TE families with unexpected differences in piRNA amounts (underexpressed with more piRNAs in D. buzzatii, overexpressed with more piRNAs in D. koepferae) are also indicated, with an arrow in some cases. No deregulated TEs are depicted in light gray. From Romero-Soriano et al. (2017) doi: 10.1093/gbe/evx091, reproduced under the Creative Commons Attribution Non-Commercial 3.0 Unported License (CC BY-NC 3.0).

Figure 5. Proportion of deregulated TE families of different categories in ovaries, classified according to differences (of at least 2-fold) between parental piRNA populations: (i) more piRNAs in D. buzzatii, (ii) not differentially abundant between parental species, (iii) more piRNAs in D. koepferae, and (iv) absence of piRNAs in both species. From Romero-Soriano et al. (2017) doi: 10.1093/gbe/evx091, reproduced under the Creative Commons Attribution Non-Commercial 3.0 Unported License (CC BY-NC 3.0).


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ping-pong amplification process, are overexpressed in D.buzzatii. Thus, protein divergence may underlie hybrid incompatibilities in both biogenesis and function of piRNAs. Three genes, ranked among the most divergent between parental species (Figure 7), show significant hybrid underexpression, Hen1 and SoYb involved in piRNA biogenesis (Horwich et al. 2007; Saito et al. 2007; Handler et al. 2013), and hybrid overexpression, Panx, panoramix, involved in transcriptional silencing (Yu et al. 2015), supporting the role of piRNA effector protein in piRNA production. Therefore, species differences in piRNA production could also be explained by diver-gence in their piRNA pathway effector proteins and/or differences in their coding gene expression levels.

It is known that many piRNA pathway genes evolve rapidly under positive selection, which has been attributed to a “Red Queen” host-pathogen arms race model (Daugherty and Malik 2012). This mechanism may be responsible of the elevated specific divergence between sibling species of piRNA-linked protein encoding genes. For instance, the rhino (rhi) gene encodes a heterochromatin pro-tein 1 (HP1) homolog protein (Rhi) that localizes to piRNA clusters. This gene, essential to specify piRNA clusters for piRNA biogenesis (Klattenhoff et al. 2009), contains elevated amounts of nonsynony-mous substitutions between D. melanogaster and D. simulans. Rhi protein interacts with the protein Deadlock (Del), encoded by the rapidly evolving del gene, and both genes are co-evolving generating species-specific interactions that prevent simulans Rhi to bind mela-nogaster Del (Parhad et al. 2017). In hybrids, this protein complex failure leads to reduced binding of Rhi to piRNA clusters, impair-ing piRNA biogenesis. Interestingly, Parhad et al. (2017) showed that divergence of the Rhi shadow domain (Rhi-SD) is responsible of the ability disruption of the protein to function in hybrids. Recently,

structural analyses revealed that amino acid differences in Rhi-SD between D. melanogaster and D. simulans lead to conformational change and electrostatic repulsion that prevent simulans Ri-SD to interact with D. melanogaster Del (Yu et al. 2018). Since the shadow domain shows the highest signature of positive selection (Vermaak et al. 2005), unbalanced expression of different effector-protein domains may be at the core of hybrid instabilities in transposon regu-latory expression via piRNA pathways. Moreover, drastic differences on the molecular architecture of the piRNA cluster specification com-plex between these 2 sibling species suggest that the piRNA pathway machinery shows robust adaptability to ensure host survival through silencing the invading transposons. We do not know how general this scenario can be, more species hybrids should be tested, but interest-ingly Del and Rhi proteins are among the most divergent between D. buzzatii and D. koepferae, the species studied by us (Figure 7).

Hybrid transposition may involve many complex mechanisms

We have run a long journey since early times when hybrids were considered devoid of value for evolution, whereas many significant mechanisms have been advanced to understand their evolutionary role much still remains to be accomplished. The seminal thrust of transposable element science, elicited first by McCintock in the 1940s and 1950s and rather later by a legion of researchers of the 1970s, has illuminated a path towards the evolutionary impact of biological shocks, both environmental and genomic, that we are currently fortunate to witness. Hybrid instability likely provides the best example of genomic shock, whose impact ranges from genomic incompatibility to new sources of evolutionary variability. Hybrid

Figure 7. Distribution of identity percentages between D. buzzatii and D. koepferae in silico proteomes. A total of 30 proteins involved in the piRNA pathway were identified as reciprocal best BLAST hits of their D. melanogaster orthologs (represented by vertical bars, their identity in parenthesis). For zucchini, 4 sequences were recognized as putative paralogs and named zucchini-A, -B, -C, and -D (only zucchini-A, -B, and -C are shown because zucchini-D was only identified in D. buzzatii). From Romero-Soriano et al. (2017) doi: 10.1093/gbe/evx091, reproduced under the Creative Commons Attribution Non-Commercial 3.0 Unported License (CC BY-NC 3.0).


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transposition was the phenomenon first witnessed by observers, but even now what are the key mechanisms that drives it highly chal-lenges most of the present researchers. Here, I have tried to overview some of what has been worked out in the field of transposition as a driver of evolution focusing on the research in interspecific hybrids performed in my laboratory under my direction and that of some collaborators, mainly Dr. Garcia Guerreiro.

This work is a partial revival of my former work concerning the early steps on revealing transposition increase in Drosophila hybrids, a model system pioneered by hybrid dysgenesis in intraspe-cific hybrids but which resisted to showing higher rate mobilization in interspecific animal hybrids. We finally demonstrated that mobil-ization is a general phenomenon that accompanies hybridization, but its effect depends on several factors, including the kind of TE and the genetic nature of the parental species. The discovery of the piRNA pathways has opened a new avenue of research to under-stand those driving factors of hybrid instability. In this work, I have also reported very recent work on the regulatory pathway intrica-cies of piRNAs associated with effector proteins in germinal tissue. Among other interesting outcomes, results suggest that TE deregula-tion in ovaries of Drosophila hybrids might be the result of several interacting phenomena, including incompatibilities of the piRNA pathway due to a functional divergence between parental species, hybrid misregulation of some piRNA pathway repressor genes of TE expression, and parental species differences in the amounts of TE-specific piRNA pools in maternal cytoplasms. The complexity of hybrid incompatibility through transposition cannot disregard other putative mechanisms including histone modifications that may mod-ify hybrid chromatin causing changes in TE expression. In flies and mice, it is known that one PIWI protein is located in the nucleus, showing, in Drosophila, a banding pattern on polytene chromo-somes of nurse cells, suggesting a direct interaction with chroma-tin (Le Thomas et al. 2013). Many experiments suggest that PIWI loaded with cluster-derived primary piRNAs gets into the nucleus and scans nascent TE transcripts. When a complementary transcript is found, PIWI may recruit chromatin factors such as histone methyl-transferases to deposit repressive histone methyl marks that modify chromatin sites. These modified sites assemble additional factors that repress transposon transcription. This is a plausible model and while correlation between repressive chromatin marks and silencing lacks a direct observation, it is clear that PIWI proteins underlie TE tran-scription inhibition and establish a repressive environment, which sets up a research avenue deserving attention in the near future (see Tóth et al. 2016 for a review).

Are there natural scenarios for hybrid evolution by transposition?

In evolution, no story is complete without an appropriate natural setting where evolutionary driving mechanisms could likely develop. Accordingly, several years ago I advanced a scenario which I here revive in part with some new ideas and examples that have been reported in the current literature.

Hybrid evolution often occurs in hybrid zones between mar-ginal populations. This is so because they inhabit a variety of new stressful open habitats in disturbed ecotone areas to be successfully invaded by hybrids. Yet, hybrid establishment may seem unlikely because isolation barriers (pre and postzygotic) would prevent the building up of an invasive hybrid population. These contact zones, however, provide multiple opportunities of hybridization generat-ing hybrid swarms often including few survival F1 individuals but

an abundance of F2 and backcrossed succcesful individuals. Thus, establishment of hybrids in contact zones is facilitated by great eco-logical opportunities in open new habitats combined with easiness of serial crosses among (and between) parental, F1, and F2 indi-viduals. This ecogenetic landscape sets off a runaway process that eventually establishes an array of introgressed backcrossed geno-types by natural selection. Adaptation is achieved by 2 kinds of selection: exogenous (ecological) selection to new open habitats and endogenous (purifying) selection, mainly fertility selection, against sterile and/or inviable hybrids but not against “all” hybrids as the “tension model” proposes (Barton and Hewitt 1985; discussed in Arnold 1997, p. 122–140). The variety of introgressed genotypes in hybrid zones facilitates this selective regime, favoring those hybrids that show high levels of fitness. This has been proven in Iris hybrids between I. fulva and I. brevicaulis where a high correlation exists between embryo inviability and the number of I. fulva genetic mark-ers introgressed in the progeny from I. brevicaulis-like maternal plants, suggesting that endogenous selection is acting against inter-mediate hybrid individuals, that is, those that contain the highest number of alien genetic elements (Arnold 1997). In a similar way, Rieseberg et al. (1996), working with Helianthus anomalus, found that similar linkage groups of genes exist in several artificial hybrid lines with high fertility. As stated above, these lines were obtained after a few generations of crossing, buttressing the rapid genome repatterning of these introgressed lines.

Rapidity is crucial to the establishment of hybrid lineages. It has been argued that, at least, this seems plausible in speciation by fixation of underdominant small chromosomal rearrangements that might mediate reproductive isolation and, eventually, speci-ation (Fontdevila 1992). The proposed scenario (Fontdevila 2005) is dependent upon the synchronous occurrence of, at least, 4 pro-cesses in contact zones. Namely, 1) transposon bursts fuel genome reorganization by increasing levels of genome transpositions and point insertions, 2) exogenous selection allows the establishment of some high fitness hybrid genotypes, 3) endogenous selection favors reorganized genomes that show high fertility and viability, and 4) small effective population size of the hybrid zone increases fixation by drift. Although much experimental evidence has been reported for each of these processes, the simultaneous occurrence of them often escaped to observation in nature and it is based on scattered, but gradually increasing, reports. Several decades ago Shaw et al. (1993) showed a natural correlation between clinal and hybrid observations of chromosomal reorganizations in 2 subspe-cies of the grasshopper Caledia captiva. Interestingly, they were able to rapidly generate chromosomal rearrangements in experimental crosses and backcrosses. Since similar chromosomal rearrangements were observed in a Caledia natural hybrid zone, they hypothesize that this experimental chromosomal instability might occur in nature as well. Moreover, the putative selective value of transposon-mediated heterochromatic rearrangements is being assessed in alti-tudinal clines of barley populations (Kalendar et al. 2000).

The role of marginal populations in the completion of hybrid evolution by transposition is crucial. Transposition bursts of TEs do likely occur permanently in natural, small marginal popula-tions under environmental and genomic stress. Belyayev (2014) extensively explains how these bursts may influence subsequent generations throughout mutations, epigenetic alterations, and quantitative and qualitative changes in TE landscape. His model emphasizes the action of burst-purification cycles that equilibrate TE copy numbers by a combination of purifying selection and drift. Ectopic recombination encompasses the whole highly repetitive


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DNA depleting tandem-repeats in marginal populations of Aegilops speltoides (Raskina et al. 2011) mostly in heterochromatic zones. Changes in chromatin due to TE transposition in hybrids were early documented (Michalak 2009). For instance, in wallabies (kanga-roo species) hybrids show extended centromeres containing many highly repeated copies of a novel retroviral element and amplifica-tion of some satellite sequences, changes in chromatin structure, and de novo whole-arm rearrangements (O’Neill et al. 1998; Metcalfe et al. 2007). Activation of TEs co-occur with centromere repattern-ing (O’Neill et al. 1998; Dimitri and Junakovic 1999) and with new rearrangements (Naveira and Fontdevila 1985; Kidwell and Lisch 1997; see Delprat et al. 2009, for a general review). New piRNA pathway studies discussed above underlie all these circumstantial observations and give support to a theory of genome-shock depend-ent hybrid evolution by transposition. Parhad et al. (2017) speculate that even adaptive evolution of piRNA pathway genes may lead to incompatibilities that disrupt piRNA function in hybrids, generat-ing general global bursts of transposition, these incompatibilities, caused by the ongoing arms race under the “Red Queen” hypothesis between transposons and the piRNA pathway, facilitate speciation not only by building reproductive barriers, but also by promoting new variability as substrate for natural selection.

Ever since McClintock (1950) proposed her early insight on the evolutionary role of genomic shocks as inducers of TE release, there has been a steady increase of natural reports on the induction of TE activity by various forms of stress (Wessler 1996; Grandbastien 1998; Garcia Guerreiro 2012; Belyayev 2014). Here, I have dealt with hybridization as a biotic stressor but other stressors includ-ing not only biotic (i.e., inbreeding) but also abiotic (i.e., heat and cold shock, UV and gamma radiation) are important. Some cases of rapid evolutionary changes have been explained by the transpos-ition burst hypothesis coupled with several of these stressors. For example,Cradock (2016) discusses the genetic paradox of the pro-fuse species-rich adaptive radiations on islands, exemplified by many colonizing lineages of animals and plants. Perhaps a most spectacu-lar example is found in the Hawaiian archipelago, where an esti-mated 1000 drosophilid endemic species, about one fourth of all described world drosophilids (Bachli 2015), originated 25 Mya from a single founder in these islands. Namely, she attempts to answer the question: why there are so many species in several island line-ages evolved from a reduced amount of colonizers? These radiations may look like a most unlikely event because the severe bottleneck of founder events and the effect of inbreeding depression, coupled with a stressful environment, would predict low evolutionary poten-tial leading to extinction rather than rapid adaptive speciation. The theory of founder effect speciation sponsored by Mayr’s concept of genetic revolutions (Mayr 1954) and modified by Carson’s flush-crash events of successive genetic reorganizations (Carson 1982, 1989) has remained obscure and contentious in the present genomic era. Craddock’s hypothesis provides a mechanism to explain these genomic revolutions and reorganizations based on repeated bursts of transposition as major triggers of these revolutions. In Hawaii, biotic stressors are inbreeding associated with founder events and hybridization between genetically divergent population isolates sep-arated by lava barriers, and abiotic stressors are heat stress from adjacent lava and toxic chemicals in volcanic gas plumes. This scen-ario includes the classical ecological shift release to an unoccupied adaptive zone (Schluter 2000, 2001), as a sequential rather than an initiating role in founder effect speciation and adaptive radiation. Some of the predictions following this scenario are accomplished. A corollary of elevated levels of TE and genome remodeling is the

expectation of higher rates of evolution and speciation. This is true for many Hawaiian plants and animals, including the silversword plant alliance, crickets of the genus Laupala and also Drosophila flies. Besides, Hawaiian Drosophila species have larger genome sizes than related species that evolved on continental islands or continents due to massive amplifications of TEs induced by stress (Chenais et al 2012; Belyayev 2014). Finally, another prediction is that TE copy number should be higher in genomes of the younger members of a lineage that have dispersed to new active islands as they arose from the ocean floor. Hunt and colleagues (Hunt et al 1984; Wisotzkey et al. 1997) confirmed this prediction for several TEs in flies of the picture wing clade of Hawaiian Drosophila.

The role of hybrid shock in restructuring genomes is actively studied in animals and plants focusing in epigenetic changes (Greaves et al. 2015), chromatin compactation, methylation (Zhu et al. 2017) and other molecular processes, such as those reported above, that could modify gene expression. In all these studies, TEs play an important role but their impact still is far from precise evalu-ation. Since the origin of genome restructuring can be elicited by several shocks, genomic and/or environmental, and its evolutionary success is dependent on population variables including deme struc-ture and frequency of occurrence, the plausible scenario is a com-plex one (Figure 8). It requires that many variables coexisted. Yet, many evolutionary changes, including introgressions, radiations and rapid speciations throughout hybridization, which long wait for an ultimate explanation, may now be assessed on the light of biological shocks coordinated with harsh ecological environments. Time soon will be ripe to propose a new scenario where some long disregarded events, hybridization prime among them, will occupy the place they deserve in evolution.

Conclusions

Barbara McClintock’s great insight foresaw the prime role of TEs in evolution when she posited in 1980: “Since the types of genome restructuring induced by such (TE) elements know few limits, their extensive release, followed by stabilization, would give rise to new species or even genera.” Though this statement was considered too far-fetched by most evolutionists of the time, empirical research in evolution has bolstered up her ideas ever since. As an example, here, I described some genome restructures induced by TE transposition through species hybridization that unleashed future evolution of many lineages. Ironically, species hybridization, a process also con-sidered of low evolutionary value by early neodarwinists, is also dis-cussed here as a trigger of transposition bursts that may drive further evolution under appropriate natural conditions. Ironically, 2 for-merly considered almost irrelevant evolutionary processes, namely TE transposition and interspecies hybridization, are merging here to likely eliciting a powerful genome restructuring for speciation and, in general, future evolution.

The journey from early glimpses to present evidences of related-ness between interspecific hybridization, transposition bursts, gen-omic rearrangements, and phenotypic novelties of adaptive value has been, and still is, a steady and, at times, harsh endeavor. Since early evidence of transposition bursts in Drosophila species hybrids, a quite frequent observation in plants but not so commonly observed in animals, to the demonstration that this was a genome-wide phe-nomenon, we had to wait the development of cutting-edge tech-nologies such as transposon display and genomic bioinformatics. Even then many details were unknown, such as that transposition


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response to genomic shock is partially dependent on TE class, on degree of introgression (backcross generation) and on other factors related to the studied hybrid progeny (family). These unknowns, however, could only be unveiled by working out the molecular mech-anisms that trigger transposition release in hybrids.

Further experiments in Drosophila ovarian TE expression showed that, although there is a bias towards overexpression, this is not the general outcome ensuing hybridization because underexpression is also present, which suggests that other factors are involved in transposition release. In ovaries of hybrids, TE deregulation is likely the product of differences between parental

Piwi-interacting RNA populations together with some differences in piRNA pathway proteins, although differences in the amounts of TE-specific piRNAS between maternal cytoplasms cannot be disregarded. These important clues notwithstanding, the take away message is that mechanisms underlying the genomic shock of hybridization as drivers of transposon release are complex and far from complete understanding. Recent empirical studies in model species on the intricacies of piRNA pathways are providing new insights and promise to improve technological advances towards genome manipulations that could generate in vitro novelties mim-icking natural hybrid species.

Modeling natural scenarios of hybrid speciation is the ultimate step of any inclusive theory of hybrid genome evolution and no scenario is complete if does not include genetic and ecological com-ponents. Hybridization is not always a dead end, rather often, it is a potential source of new arrays of hybrids (dubbed “hybrid swarms” by specialists) that may eventually establish themselves in new eco-tone habitats, and evolve as new species. Moreover, the proposed scenario is dependent upon the synchronous occurrence of TE trans-position bursts with selection (endogenous and exogenous) and fix-ation of some hybrid arrays helped by drift in small demes found in hybrid zones. This scenario may seem complex and unassailable but nature, an “entangled bank” subject to natural selection as seen by Darwin or a seemingly random, chaotic, and unassailable melee for occasional observers, is, however, a structured building governed by fully explicable laws that weave the tissue of evolution. Here, hybrid speciation fueled by TE transposition seems to be an import-ant fact of evolution and no doubt disentangling it is a worth, and feasible, attempt.

Supplementary Material

Supplementary data are available at Journal of Heredity online.

Funding

This work was supported by Grant CGL2017-89160P from Ministerio de Economía y Competitividad, Spain; and Generalitat de Catalunya, Spain (2017SGR 1379).

AcknowledgmentsParts of the article from reference Fontdevila (2005) are reproduced here with permission from S. Darger AG, Basel publishers. Other parts, including fig-ures and tables, from references Vela et al. (2014) and Romero-Soriano (2017) are reproduced here under the Creative Commons Attribution International Licenses CC BY 4.0 and CC BY-NC 3.0, respectively. I want to thank María Pilar Garcia Guerreiro for her valuable discussions and ideas after revising a draft of this manuscript. I also want to thank 2 anonymous reviewers for their helpful comments. I am very grateful to Therese Markow for inviting me to the international 2018 AGA-sponsored meeting in Alamos, Sonora (Mexico) on the “ Evolutionary Genetics and Ecology: The Cactophilic Drosophila Model System.”

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Figure 8. Natural scenario of hybrid genome evolution by transposition. The initial (upper) part of the chart depicts how interspecific hybridization promotes genome instability due to epigenetic changes and divergence in piRNA pathways. Genome instability is defined by high transposition rates that induce high mutation rates, new rearrangements, new gene expression, and ectopic recombination. The middle part shows how the ensuing hybrid genome reorganization is stabilized by drift fixation and natural selection (endogenous and exogenous). These processes may lead to adaptation (the lower part) either by ecological release occupation of novel environments, new ecotones in many cases, or by replacement of parental species. The final step of this scenario is reticulate evolution by introgression or the evolution of a new species.


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