All the instructions required for life are encoded in the set of DNA present in a cell. It therefore seems natural to think that every bit of this genetic information should serve the organism. And yet most species carry parasitic ‘transposable’ sequences, or transposons, whose only purpose is to multiply and insert themselves at other positions in the genome.

It is possible for cells to suppress these selfish elements. Chemical marks can be deposited onto the DNA to temporarily ‘silence’ transposons and prevent them from being able to move and replicate. However, this sometimes comes at a cost: the repressive chemical modifications can spread to nearby genes that are essential for the organism and perturb their function.

Strangely, the prevalence of transposons varies widely across the tree of life. These sequences form the majority of the genome of certain species – in fact, they represent about half of the human genetic information. But their abundance is much lower in other organisms, forming a measly 6% of the genome of puffer fish for instance. Even amongst fruit fly species, the prevalence of transposable elements can range between 2% and 25%. What explains such differences?

Huang et al. set out to examine this question through the lens of transposon silencing, systematically comparing how this process impacts nearby regions in six species of fruit flies. This revealed variations in the strength of the side effects associated with transposon silencing, resulting in different levels of perturbation on neighbouring genes. A stronger impact was associated with the species having fewer transposons in its genome, suggesting that an evolutionary pressure is at work to keep the abundance of transposons at a low level in these species. Further analyses showed that the genes which determine how silencing marks are distributed may also be responsible for the variations in the impact of transposon silencing. They could therefore be the ones driving differences in the abundance of transposons between species.

Overall, this work sheds light on the complex mechanisms shaping the evolution of genomes, and it may help to better understand how transposons are linked to processes such as aging and cancer.

Transposable elements (TEs) are widespread genetic parasites that copy and insert themselves across host genomes. The presence and movement of TEs could impair host genome functions. TEs disrupt genes and functional elements (Finnegan, 1992), introduce ectopic regulatory sequences (Chuong et al., 2017), and trigger highly deleterious chromosomal rearrangements through nonhomologous recombination (Langley et al., 1988; Montgomery et al., 1991). Nevertheless, the ability to self-replicate has allowed TEs to successfully occupy nearly all eukaryotic genomes surveyed (reviewed in Wells and Feschotte, 2020). Within a eukaryotic genome, TEs are prevalent in both gene-poor, repeat-rich heterochromatic and gene-rich euchromatic regions (e.g., Kaminker et al., 2002; Bergman et al., 2006). TEs in the heterochromatic genome are oftentimes fragmented, losing their ability to replicate (e.g., Hoskins et al., 2007; Hoskins et al., 2015). On the contrary, euchromatic TEs, which could intersperse with functional elements, commonly retain the potential to replicate, making them active players for not only their own evolutionary dynamics, but also the function and evolution of the euchromatic genome. Because of that and the technical challenges associated with identifying TEs in the heterochromatic regions (Salzberg and Yorke, 2005; Treangen and Salzberg, 2011), studies have been largely focused on the evolution of TEs in the euchromatic genome. Intriguingly, the abundance of TEs in the euchromatic genome substantially varies across the phylogenetic tree (Huang et al., 2012; Elliott and Gregory, 2015; Wells and Feschotte, 2020). For instance, in the assembled vertebrate genomes, which mostly consist of euchromatic regions, the proportion occupied by TEs ranges from only 6% in pufferfish (Volff et al., 2003) to more than 65% in salamander (Nowoshilow et al., 2018). Even within the same genus, genomic TE abundance differs widely (e.g., 2.5–25% of assembled genome sequences in Drosophila; Clark et al., 2007; Rius et al., 2016). Deciphering the role of this prevalent parasite in shaping genome evolution has remained a central question in genomics (Kazazian, 2004; Feschotte and Pritham, 2007; Arkhipova and Kumar, 2018); however, the ultimate causes of such dramatic divergence in TE abundance in the euchromatic genome remain unclear.

Theoretical analyses proposed that, in panmictic host populations with unrestricted recombination, TE abundance is determined by how quickly TEs replicate and how fast they are removed from the populations by natural selection against their harmful fitness effects (Charlesworth and Charlesworth, 1983, reviewed in Lee and Langley, 2010). Under this model, divergent genome-wide TE abundance could be driven by between-species differences in the strength of selection against TEs. Currently available evolutionary models that address this possibility have focused on population genetic parameters that influence the efficacy of selection removing TEs, such as mating systems (Wright and Schoen, 1999; Dolgin and Charlesworth, 2006; Boutin et al., 2012) and effective population size (Lynch and Conery, 2003). Yet, empirical support for such a hypothesis has been mixed (Dolgin et al., 2008; Lockton and Gaut, 2010; de la Chaux et al., 2012; Arunkumar et al., 2015; Agren et al., 2014; Mérel et al., 2021; Oggenfuss et al., 2021). On the other hand, between-species differences in the magnitude of harmful effects exerted by TEs, and accordingly the strength of selection against TEs, could also determine genomic TE abundance, a plausible hypothesis that is yet to have empirical investigations.

A new avenue for exploring how these genetic parasites shape the function and evolution of eukaryotic genomes was opened by the recently discovered host-directed silencing of TEs and the associated ‘inadvertent’ deleterious epigenetic effects (reviewed in Choi and Lee, 2020). To counteract the selfish increase of TEs in host genomes, eukaryotic hosts have evolved small RNA-mediated mechanisms to transcriptionally silence TEs (reviewed in Slotkin and Martienssen, 2007; Czech et al., 2018; Deniz et al., 2019). Host protein complexes are guided by small RNAs to TEs with complementary sequences, which is followed by the recruitment of methyltransferases that modify DNA or histone tails at TE sequences (Qi et al., 2006; Aravin et al., 2008; Wang and Elgin, 2011; Sienski et al., 2012; Le Thomas et al., 2013). Such a process results in the enrichment of DNA methylation or di- and tri-methylation on lysine 9 of histone H3 (H3K9me2/3), both repressive epigenetic modifications that are typically found in heterochromatic regions and associated with repressed gene expression (reviewed in Pikaard and Mittelsten Scheid, 2014; Allis and Jenuwein, 2016). This repressed transcription of TEs results in reduced RNA intermediates (for RNA-based TEs) and proteins (e.g., transposase and reverse transcriptase) necessary for TE replication, effectively slowing the selfish propagation of TEs.

While such epigenetic silencing of TEs should benefit their hosts, studies in various model species have found that repressive marks enriched at silenced TEs ‘spread’ beyond TE boundaries, leading to local enrichment of such marks at TE-adjacent sequences across the euchromatic genomes (i.e., Mus, Drosophila, Arabidopsis, and Oryza; Rebollo et al., 2012; Sienski et al., 2012; Pezic et al., 2014; Lee, 2015; Quadrana et al., 2016; Choi and Purugganan, 2018, reviewed in Choi and Lee, 2020). Furthermore, TEs with such effects were observed to have lower population frequencies (Hollister and Gaut, 2009; Lee, 2015; Lee and Karpen, 2017), suggesting that selection acts to remove them. These discoveries highlight the potential importance of TE-triggered epigenetic effects in shaping genome evolution. Interestingly, the strength of TE-mediated local enrichment of repressive marks substantially varies between distantly related taxa (reviewed in Choi and Lee, 2020). Investigations on pairs of closely related species further revealed that this ‘epigenetic effect of TE’ differs and is stronger in the species with fewer euchromatic TEs (Arabidopsis thaliana vs. Arabidopsis lyrata and Drosophila melanogaster vs. Drosophila simulans; Hollister et al., 2011; Lee and Karpen, 2017). These observations spurred our previous hypothesis that, across species, different TE-mediated enrichment of repressive marks could result in varying functional consequences and thus differences in the strength of selection against TEs, eventually contributing to divergent TE abundance in the euchromatic genome (Lee and Karpen, 2017). We further postulated that this difference in TE-mediated epigenetic effects could have resulted from species-specific genetic modulation of the repressive chromatin landscape (Lee and Karpen, 2017), which was shown to determine the spreading of repressive epigenetic marks from constitutive heterochromatin into adjacent euchromatic sequences (reviewed in Girton and Johansen, 2008; Elgin and Reuter, 2013).

To fully examine the hypothesis that varying host chromatin landscape drives between-species differences of TEs through epigenetic mechanisms, one needs to connect species-specific regulation of chromatin landscape, TE-mediated enrichment of repressive marks, the associated functional consequence and resultant selection against TEs, and genomic TE abundance. However, former analyses that compared TE-mediated epigenetic effects between species have limited sampling (two species) and thus lack sufficient statistical power for robust inference (Hollister et al., 2011; Lee and Karpen, 2017). Also, support for key links of the hypothesis is lacking. For instance, selection against TE-mediated epigenetic effects was expected to result from the associated reducing effects on the expression of neighboring genes. Yet, investigations in multiple taxa reported weak or no associations between the epigenetic effects of TEs and neighboring gene expression (Quadrana et al., 2016; Stuart et al., 2016; Lee and Karpen, 2017; Choi and Purugganan, 2018, reviewed in Kelleher et al., 2020; Choi and Lee, 2020). These inconclusive observations cast doubt on the possibility that TE-mediated epigenetic effects impair host fitness by silencing neighboring genes and whether this particular deleterious consequence indeed shapes genome evolution. Furthermore, previous comparisons of population frequencies between TEs with and without epigenetic effects, an approach used to infer the strength of natural selection removing TEs, could not exclude the confounding influence of other harmful effects of TEs on their population frequencies (e.g., Hollister and Gaut, 2009; Lee, 2015). Accordingly, those analyses could not unequivocally support selection against TE-mediated epigenetic effects. Multi-species studies that span an appropriate evolutionary distance and connect the missing links in the proposed hypothesis would be needed to test the predicted importance of TE-mediated epigenetic effects in determining between-species differences of TEs.

In this study, we investigated the prevalence of TE-mediated local enrichment of repressive epigenetic marks, or ‘TE-mediated epigenetic effects’, in the euchromatic genome of six species in the D. melanogaster subgroup (diverged around 10 MYR; Obbard et al., 2012, Figure 1A). These species are from the two well-studied species complexes (melanogaster and yakuba complexes), providing good phylogenetic resolution to address the role of TE-mediated epigenetic effects in genome evolution. While TE insertions in all species studied result in robust local enrichment of repressive epigenetic marks, the strength of such effects varies substantially within genomes, among species, and between species complexes. Our larger sample size allowed us to re-examine the still debated question about the impacts of TE-mediated enrichment of repressive marks on neighboring gene expression, which surprisingly revealed their complex interactions. Importantly, our multi-species analysis provides the power to test the predicted associations between TE abundance in the euchromatic genome, TE-mediated epigenetic effects, selection against such effects, and host chromatin environment, while uncovering the evolutionary causes for the wide variety of TE abundance between species.

Figure 1 with 8 supplements see all

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The replicative nature of TEs has made them successful at occupying nearly all eukaryotic genomes. Yet, their ‘success’, or genomic abundance, drastically varies across the phylogenetic tree (Huang et al., 2012; Elliott and Gregory, 2015; Wells and Feschotte, 2020) and between closely related species (Hu et al., 2011; Rius et al., 2016; Legrand et al., 2019), raising important questions regarding the evolutionary causes and functional consequences of varying genomic TE abundance. It is worth noting that most studies about the evolution of TE abundance, including ours, mainly concern insertions in the euchromatic genome. Although TEs are highly abundant in the heterochromatic genome, these TEs are typically fragmented (Hoskins et al., 2007; Hoskins et al., 2015) and would no longer be part of the ‘life cycle’ of TEs. The role of euchromatic TEs in determining the abundance and evolutionary dynamics of TEs in the heterochromatic genome is still a largely unaddressed question, mainly due to the challenges associated with assembling TEs in repeat-rich heterochromatic sequences (Salzberg and Yorke, 2005; Treangen and Salzberg, 2011, but see Khost et al., 2017; Chang and Larracuente, 2019; Chang et al., 2019).

Several hypotheses have been proposed to explain the large variation in euchromatic TE abundance. Phylogenetic signals may explain some of the differences between distantly related taxa (Wells and Feschotte, 2020) and, sometimes, between species within a taxa (Szitenberg et al., 2016). Variation in TE activities was also postulated to contribute to the wide variability of TE abundance (Chen et al., 2019; Wong et al., 2019, but see Ho et al., 2021). Still another plausible cause is systematic differences in the strength of natural selection removing TEs between species. Investigations of this hypothesis have been largely focused on population genetic parameters that influence the efficacy of natural selection, such as mating systems (Wright and Schoen, 1999; Dolgin et al., 2008; Boutin et al., 2012; Arunkumar et al., 2015; Agren et al., 2014) and effective population size (Lynch and Conery, 2003; Mérel et al., 2021). Here, our multi-species study tested step-by-step yet another evolutionary mechanism by which the strength of selection removing TEs could differ—through differences in the epigenetic effects of TEs that are driven by species-specific host chromatin landscape.

In this study, we investigated the prevalence, variability, and evolutionary importance of ‘the epigenetic effects of TEs’—TE-mediated local enrichment of repressive epigenetic marks—in the euchromatic genomes of six Drosophila species. These species come from two important and well-studied complexes within the melanogaster species subgroup (melanogaster and yakuba complexes), providing good phylogenetic resolution to decipher the evolutionary role of epigenetic mechanisms in shaping species-specific TE abundance. We observed that TE-mediated local enrichment of repressive marks is prevalent in all species studied and widely varies both within and between genomes. Interestingly, in addition to the intrinsic biological properties of TEs, our analyses revealed that host genetic background plays a critical role in determining the strength of TE-mediated epigenetic effects. These TE-mediated enrichments of repressive marks alter the epigenetic states of neighboring euchromatic sequences, including actively transcribing genes. Importantly, TEs exerting such epigenetic effects are selected against across multiple species, and the strength of this TE-mediated epigenetic effect negatively correlates with genomic TE abundance within species complex. Our findings extend previous studies based on few species and provide one of the first support for the importance of the inadvertent harmful effects of TE epigenetic silencing in shaping divergent genomic TE landscapes.

Curiously, we only found a negative association between genomic TE abundance and the magnitude of TE-mediated H3K9me2 enrichment across species, but not the extent of the spreading, even though these two indexes of a TE significantly correlate within genomes (Figure 1—figure supplement 2). Similarly, the evidence for selection against TE-mediated epigenetic effects is stronger for the magnitude of TE-induced H3K9me2 enrichment than for the extent (Figure 4). Previous empirical (Belyaeva and Zhimulev, 1991; Talbert and Henikoff, 2000) and theoretical (Erdel and Greene, 2016) studies have suggested that the spreading of repressive heterochromatic marks is a nonlinear process. Accordingly, the extent of the spreading of repressive marks from TEs could be sensitive to the genomic context and subject to substantial stochasticity. This echoes our observations that the transcription of genes influences the extent of TE-mediated H3K9me2 spreading, but not the magnitude of H3K9me2 enrichment (Figure 3D and Figure 3—figure supplement 10; also see below). The magnitude of TE-mediated H3K9me2 enrichment, which is estimated in windows right next to TE boundary, may thus be a more direct measurement of the strength of TE-mediated epigenetic effects and more indicative of the associated harmful impacts.

One of our most surprising findings is perhaps the limited evidence in supporting that TE-mediated epigenetic effects reduce neighboring gene expression on a genome-wide scale. While TE-mediated epigenetic effects increase the enrichment of repressive epigenetic marks at adjacent genes, we found limited associations between such effects and gene expression within genomes (Figure 3A and B). Comparing the expression of homologous alleles with and without TEs showing epigenetic effects also reached the same conclusion (Figure 3C). These observations echo previously reported lack of genome-wide associations between TE-induced enrichment of repressive epigenetic marks and the expression of neighboring genes in several model organisms (Quadrana et al., 2016; Stuart et al., 2016; Lee and Karpen, 2017; Choi and Purugganan, 2018) and are consistent with the wider observation that TEs upstream or downstream to genes are not predominantly associated with reduced gene expression (Goubert et al., 2020; Ullastres et al., 2021; Rech et al., 2022, reviewed in Kelleher et al., 2020; Choi and Lee, 2020). The limited impacts of TE-mediated H3K9me2 enrichment on gene expression could have resulted from the complex relationship between repressive epigenetic modification and gene expression (de Wit et al., 2007; Yasuhara and Wakimoto, 2008; Riddle et al., 2011; Meng et al., 2016; Caizzi et al., 2016), the varying sensitivity of genes to the enrichment of repressive marks (Rudolph et al., 2007; Vogel et al., 2009; Riddle et al., 2011), and the presence of other types of variants that also modulate gene expression (Stranger et al., 2007). Interestingly, our findings suggested another possibility—the transcription of genes, in return, influences TE-mediated epigenetic effects across genomes. Specifically, we found a more restricted spreading of repressive marks from TEs on the side facing a gene than on the intergenic side, and this difference is mainly observed for TEs near the promoters of highly expressed genes (Figure 3—figure supplement 12). It is worth noting that this difference in the extent of H3K9me2 spreading between the two sides of a TE is unlikely driven by the presence of insulator sequences (Gaszner and Felsenfeld, 2006) because of the limited associations between the presence of insulator sequences and the reduction in TE-mediated H3K9me2 spreading on the genic side (Figure 3—figure supplement 13). On the other hand, active histone modifications enriched at transcriptionally active genes could antagonize the assembly of heterochromatin (Allshire and Madhani, 2018), potentially restraining the spreading of repressive marks from silenced TEs. Consistently, in mice, active histone modification was reported to spread from an actively transcribing candidate gene into an adjacent TE (Rebollo et al., 2012). Similarly, active gene transcription at Drosophila miranda neo-Y chromosome was found to impede the formation of heterochromatin (Wei et al., 2020). Future analysis of the distributions of active histone modifications may help reveal the mechanistic cause for our observed genome-wide dependencies of the extent of TE-mediated epigenetic effects on the transcriptional activities of adjacent euchromatic genes.

If not due to reducing the expression of adjacent genes, what functional consequences of TE-mediated epigenetic effects could have impaired host fitness and led to the observed selection against these TEs? Euchromatic TEs enriched with repressive epigenetic marks were reported to spatially interact with constitutive heterochromatin through phase separation mechanisms, a process observed to alter 3D structures of genomes and inferred to lower host fitness (Lee et al., 2020). In addition, the epigenetic effects of TEs could shift the usual DNA repair process in the gene-rich euchromatic genome, perturbing the maintenance of local genome integrity. This is because double-stranded breaks happening in constitutive heterochromatin are repaired through a distinct cellular process from those in the euchromatic genome, owing to the enrichment of repressive epigenetic modifications (Chiolo et al., 2011; Janssen et al., 2016; Janssen et al., 2019). Still, the variance of gene expression was shown to be shaped by natural selection (Metzger et al., 2015; Duveau et al., 2018). Given the variegating properties of the spreading of repressive marks (reviewed in Elgin and Reuter, 2013), TE-mediated epigenetic effects could have shifted the variance, instead of the mean, of neighboring gene expression, impacting host fitness.

Building upon our findings of the prevalence and variability of TE-mediated epigenetic effects and selection against such effects, our multi-species analysis provides strong support for the previously proposed role of TE-mediated epigenetic effects in determining genomic TE abundance (Figure 6). This interpretation is based on the assumption that TE copy number is at equilibrium and transposition rates of TEs are similar across species, leaving the strength of selection removing TEs being the major determinant of genomic TE abundance (Charlesworth and Charlesworth, 1983). By combining transcriptomic analysis and Drosophila genetics experiment, we further revealed that between-species differences in TE-mediated epigenetic effects could be driven by species-specific expression levels of host genetic factors that modulate heterochromatin. These findings connect the evolution of host genome (genomic TE abundance) with chromatin landscape through the inadvertent harmful effects of the epigenetic silencing of TEs (Figure 6). Curiously, the negative association between TE-mediated H3K9me2 enrichment and genomic TE abundance was only observed within species complex, pointing that the importance TE-mediated epigenetic effects in determining genomic TE abundance may be on a short evolutionary time scale. Specifically, even though we found stronger epigenetic effects of TEs in species of the yakuba complex than those in the melanogaster complex, TEs are more abundant in the former. This accumulation of TEs in the genomes of yakuba complex is in line with previously observed greater net gains of intron sequences (Presgraves, 2006) and duplicated genes (Hahn et al., 2007) in D. yakuba than those in the lineage leading to melanogaster complex, which could suggest a higher tolerance of D. yakuba genome with gained sequences. Such lineage-specific mechanism that shapes the gain and loss of sequences over the entire genome may also play an important role in determining genomic TE abundance and potentially override the influence of selection against varying TE-mediated epigenetic effects on a longer evolutionary time scale.

Figure 6

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It is worth noting that teasing apart the causality of the observed associations between the epigenetic effects and genomic abundance of TEs is challenging. A reduction in effective population size and accordingly weakened effectiveness of natural selection at removing TEs could drive the accumulation of TEs in some of the species (e.g., Mérel et al., 2021). Under this scenario, selection may favor epigenetic regulation that limits excessive inadvertent spreading of repressive marks from euchromatic TEs, which could also result in our observed weaker TE-mediated epigenetic effects in species with abundant TEs. Moreover, even if the difference in genomic TE abundance is indeed the ‘consequence’, varying efficacy of selection in purging deleterious TE insertions could also contribute to the observed between-species difference in TE abundance. Specifically, within species complex, estimated nucleotide polymorphism, an indicator for effective population size (Charlesworth, 2009), largely follows a similar rank order to our observed magnitude of TE-mediated H3K9me2 enrichment (nucleotide polymorphism, melanogaster complex: D. simulans > D. mauritiana > D. melanogaster (Langley et al., 2012; Meiklejohn et al., 2018) and yakuba complex: D. tessieri > D. yakuba > D. santomea (Bachtrog et al., 2006); the only difference in the rank order being the epigenetic effect of TEs is stronger in D. mauritiana than in D. simulans, Figure 5A). More effective selection at removing TEs in species with larger effective population size (but also stronger epigenetic effects of TEs) is another plausible driver for varying TE abundance that our analysis could not rule out.

Our study focuses on late-stage embryos and would capture the averaged epigenetic effects of TEs across heterogeneous cell types at this developmental stage. If TE-mediated epigenetic effects vary minimally across tissues or cell types, our estimate serves as a good proxy to study the associated fitness consequence. Yet, if TE-mediated enrichment of repressive marks substantially varies between tissues and cell types that have different importance in shaping individual functions, our estimate could fail to capture the most relevant variation in TE-mediated epigenetic effects that determine individual fitness. Even though we did find evidence supporting selection against TE-mediated enrichment of repressive marks that was estimated from whole embryos, future investigation on the variability of such effects across tissues and cell types will be important for the finer dissection of the role of TE-mediated epigenetic effects in individual fitness and, thus, genomic TE abundance.

Proper maintenance of heterochromatin ensures genome function and integrity (reviewed in Janssen et al., 2018). Intriguingly, the expression level (see above), copy number (Levine et al., 2012; Ross et al., 2013; Helleu and Levine, 2018), and amino acid sequences (Levine et al., 2012; Sasaki et al., 2019) of heterochromatin structural and enzymatic components have been observed to vary substantially within and between species. The abundance and composition of heterochromatic repeats also rapidly turnover between genomes (Larracuente, 2014; Wei et al., 2014; Wei et al., 2018). While variation in these genetic factors was postulated to contribute to the evolution of heterochromatin functions (e.g., Ferree and Barbash, 2009; Helleu and Levine, 2018; Mills et al., 2019), our discoveries further extend their evolutionary impacts from the gene-poor genomic dark matter into the gene-rich euchromatin. Heterochromatin modulators may not only determine the local epigenetic impacts of euchromatic TEs on flanking sequences, but also shape TE abundance and, accordingly, the structure and function of the euchromatic genomes. The evolution of euchromatin and heterochromatin, two genomic compartments usually presumed to function independently, may be more interconnected than previously thought by the inadvertent deleterious epigenetic effects of a widespread genetic parasite.

Short-read data for ChIP-seq, RNA-seq, and Illumina whole-genome sequencing have been deposited to NCBI BioProject under accession number PRJNA855483. PacBio long-read data and genome assembly of D. melanogaster ORw1118 strain have been deposited to NCBI BioProject under accession number PRJNA855235.

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Author details

1. Yuheng Huang

   Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, United States

   Contribution

   Data curation, Formal analysis, Validation, Investigation, Methodology, Writing - original draft, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1586-953X

2. Harsh Shukla

   Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, United States

   Contribution

   Software, Writing - review and editing

   Competing interests

   No competing interests declared

3. Yuh Chwen G Lee

   Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, United States

   Contribution

   Conceptualization, Resources, Data curation, Formal analysis, Supervision, Funding acquisition, Investigation, Visualization, Methodology, Writing - original draft, Project administration, Writing - review and editing

   For correspondence

   grylee@uci.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-0081-7892

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