Genome Reduction: Does size really matter?

Analysis of the smallest known arthropod genome reveals a mechanism for genome reduction that appears to be driven by a specialized ecological interaction with plants.
  1. David G Heckel  Is a corresponding author
  1. Department of Entomology, Max Planck Institute for Chemical Ecology, Germany

When it comes to animals, the saying ‘the bigger the better’ does not always hold true. Being small comes with some advantages, such as needing fewer resources or having more opportunities to hide or escape from predators. Take, for example, the tomato russet mite Aculops lycopersici, which is a pest that can cause serious damage to tomatoes and other related plants (including potatoes, tobacco and various peppers), even though it is among the tiniest animals on Earth and smaller than some single-celled organisms.

The tomato russet mite feeds on the outer epidermal cells of plant leaves by piercing the cell wall, secreting proteins and other compounds into the cell, and then sucking out the contents (Figure 1). Many plants rely on the jasmonic acid pathway to turn on their defenses against mites and other herbivores (Howe and Jander, 2008), but Aculops and other tomato-feeding mites can inhibit this pathway, although the mechanisms they use to do this remain unknown (Schimmel et al., 2018).

Mites on a leaf.

A spider mite (brown, left) towers above two russet mites (white, right) among the trichomes of a tomato leaf. Both species can suppress the signaling pathways used by the plant to upregulate anti-herbivore defenses, but it remains unclear how tomato russet mites do this.

Image Credit: Jan van Arkel (IBED, University of Amsterdam) from Glas et al., 2014 (CC BY 4.0).

Comparative genomics of chelicerates – a large group of arthropods to which the tomato russet mite belongs – has already revealed significant differences to insects and could hold the clue to why these mites are such successful crop pests. Now, in eLife, Merijn Kant (University of Amsterdam), Richard Clark (University of Utah) and colleagues – including Robert Greenhalgh (University of Utah) and Wannes Dermauw (Ghent University) as joint first authors – report new insights on mite genomics (Greenhalgh et al., 2020).

The researchers sequenced the genome of Aculops mites and discovered that they have the smallest known arthropod genome to date,containing just 32.5 million bases. This was attained by an extreme reduction in both DNA content and gene number, especially in gene families involved in clearing toxins and sensing chemicals. Moreover, several transcription factors (proteins that help turn on and off genes) found in almost every other eukaryote were missing from the russet mite genome: this is puzzling because the mite is free-living, with no known symbiont that might complement its deficient gene repertoire.

The extent of DNA loss points to aggressive mechanisms for trimming down the genome. The average space between genes was about 540 base pairs, so that the number of base pairs between genes was roughly equal to the number coding for proteins. Any mechanism that has evolved to remove transposable elements (DNA sequences that can change their position within the genome) could achieve this, and also be responsible for the gene loss. Indeed, transposable elements account for less than 2% of the Aculops genome.

Moreover, there was a massive loss of non-coding DNA within genes: over 80% did not have any introns –regions of DNA that interrupt the coding sequence and are ‘spliced out’ before proteins are made. Even intron positions that are highly conserved across related species were absent in the tomato russet mite. For the other 20% of genes, most had retained their introns at the 5' end, but lost them at the 3' end – a pattern that has also been observed in other intron-poor organisms (Mourier and Jeffares, 2003; Roy and Gilbert, 2005).

The mRNA from which all the introns have been spliced out can serve as the template for an enzyme called reverse transcriptase, which makes single strands of DNA that are complementary to the mRNA. This process starts from the 3' end, and the resulting DNA can be integrated into the genome at the site of the original gene, replacing the original 3' end (which had introns) with a new 3' end (which has no introns). The 5' end (and its intron) remains intact. This mechanism would seamlessly ‘erase’ some introns (replacing the genomic DNA with intron-free sequence), rather than ‘excising’ them (physically cutting them out of the genomic DNA), although Greenhalgh et al. did find a few instances of imprecise excision. The enzymes responsible for these manipulations belong to the toolkit of retrotransposons, elements that can move by copying RNA into DNA, but they have yet to be identified in the russet mite.

Although the mechanisms of genome reduction can be envisioned, the evolutionary driving force behind them remains an enigma. Plant-parasitizing mites seem to have created their own niche among herbivores by manipulating plant biochemistry in ways where a small body size is an advantage. Shielded by leaf hairs and crevices, these tiny leaf feeders remain well hidden from most predators. Some mite species even hormonally manipulate plant structures into galls that encase them. The epidermal cells in plants are also relatively poor in nutrients, putting a premium on small size and high efficiency.

Paradoxically, the extreme genome reduction of Aculops lycopersici runs counter to adaptations of most insect herbivores studied to date, which usually show great expansions in gene families relevant for sensing chemicals and destroying toxins. How this mite can manipulate a plant’s defense mechanisms continues to remain a mystery. Comparisons to other tomato-feeding mites showed few similarities in the composition of saliva proteins, which are presumed to inactivate the plant's defensive signaling pathways.

So, what scenarios could explain a tendency to minimize the genome, and could they really lead to better adaptations of the parasite? The fitness cost of gene loss might not immediately be balanced by a reduced size, but a short generation time of four days would facilitate a rapid evolutionary adjustment to compensate. Since infestations may start with one or a few dispersing individuals but then rapidly explode to huge population sizes, random genetic drift could further accelerate the process. Can (small) size matter so much to fitness to sustain the continuous and gradual erosion of DNA that ultimately shaped the russet mite of the 21st century? Unraveling the evolutionary dynamics of this process could be the greatest benefit of a comparative study of parasitic mites and their relatives.


Article and author information

Author details

  1. David G Heckel

    David G Heckel is in the Department of Entomology, Max Planck Institute for Chemical Ecology, Jena, Germany

    For correspondence
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8991-2150

Publication history

  1. Version of Record published: December 8, 2020 (version 1)


© 2020, Heckel

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.


  • 1,605
    Page views
  • 132
  • 1

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. David G Heckel
Genome Reduction: Does size really matter?
eLife 9:e64483.
  1. Further reading

Further reading

    1. Developmental Biology
    2. Evolutionary Biology
    Erliang Yuan, Huijuan Guo ... Yucheng Sun
    Research Article

    Wing dimorphism in insects is an evolutionarily adaptive trait to maximize insect fitness under various environments, by which the population could be balanced between dispersing and reproduction. Most studies concern the regulatory mechanisms underlying the stimulation of wing morph in aphids, but relatively little research addresses the molecular basis of wing loss. Here, we found that, while developing normally in winged-destined pea aphids, the wing disc in wingless-destined aphids degenerated 30-hr postbirth and that this degeneration was due to autophagy rather than apoptosis. Activation of autophagy in first instar nymphs reduced the proportion of winged aphids, and suppression of autophagy increased the proportion. REPTOR2, associated with TOR signaling pathway, was identified by RNA-seq as a differentially expressed gene between the two morphs with higher expression in the thorax of wingless-destined aphids. Further genetic analysis indicated that REPTOR2 could be a novel gene derived from a gene duplication event that occurred exclusively in pea aphids on autosome A1 but translocated to the sex chromosome. Knockdown of REPTOR2 reduced autophagy in the wing disc and increased the proportion of winged aphids. In agreement with REPTOR’s canonical negative regulatory role of TOR on autophagy, winged-destined aphids had higher TOR expression in the wing disc. Suppression of TOR activated autophagy of the wing disc and decreased the proportion of winged aphids, and vice versa. Co-suppression of TOR and REPTOR2 showed that dsREPTOR2 could mask the positive effect of dsTOR on autophagy, suggesting that REPTOR2 acted as a key regulator downstream of TOR in the signaling pathway. These results revealed that the TOR signaling pathway suppressed autophagic degradation of the wing disc in pea aphids by negatively regulating the expression of REPTOR2.

    1. Evolutionary Biology
    2. Genetics and Genomics
    Xinzhu Wei, Christopher R Robles ... Sriram Sankararaman
    Research Article

    The genetic variants introduced into the ancestors of modern humans from interbreeding with Neanderthals have been suggested to contribute an unexpected extent to complex human traits. However, testing this hypothesis has been challenging due to the idiosyncratic population genetic properties of introgressed variants. We developed rigorous methods to assess the contribution of introgressed Neanderthal variants to heritable trait variation relative to that of modern human variants. We applied these methods to analyze 235,592 introgressed Neanderthal variants and 96 distinct phenotypes measured in about 300,000 unrelated white British individuals in the UK Biobank. Introgressed Neanderthal variants have a significant contribution to trait variation consistent with the polygenic architecture of complex phenotypes (contributing 0.12% of heritable variation averaged across phenotypes). However, the contribution of introgressed variants tends to be significantly depleted relative to modern human variants matched for allele frequency and linkage disequilibrium (about 59% depletion on average), consistent with purifying selection on introgressed variants. Different from previous studies (McArthur 2021), we find no evidence for elevated heritability across the phenotypes examined. We identified 348 independent significant associations of introgressed Neanderthal variants with 64 phenotypes . Previous work (Skov 2020) has suggested that a majority of such associations are likely driven by statistical association with nearby modern human variants that are the true causal variants. We therefore developed a customized statistical fine-mapping methodology for introgressed variants that led us to identify 112 regions (at a false discovery proportion of 16%) across 47 phenotypes containing 4,303 unique genetic variants where introgressed variants are highly likely to have a phenotypic effect. Examination of these variants reveal their substantial impact on genes that are important for the immune system, development, and metabolism. Our results provide the first rigorous basis for understanding how Neanderthal introgression modulates complex trait variation in present-day humans.