skip to main content


Title: Genetic hitchhiking, mitonuclear coadaptation, and the origins of mt DNA barcode gaps
Abstract

DNA barcoding based on mitochondrial (mt) nucleotide sequences is an enigma. Neutral models of mt evolution predict DNA barcoding cannot work for recently diverged taxa, and yet, mt DNA barcoding accurately delimits species for many bilaterian animals. Meanwhile, mt DNA barcoding often fails for plants and fungi. I propose that because mt gene products must cofunction with nuclear gene products, the evolution of mt genomes is best understood with full consideration of the two environments that impose selective pressure on mt genes: the external environment and the internal genomic environment. Moreover, it is critical to fully consider the potential for adaptive evolution of not just protein products of mt genes but also of mt transfer RNAs and mt ribosomal RNAs. The tight linkage of genes on mt genomes that do not engage in recombination could facilitate selective sweeps whenever there is positive selection on any element in the mt genome, leading to the purging of mt genetic diversity within a population and to the rapid fixation of novel mt DNA sequences. Accordingly, the most important factor determining whether or not mt DNA sequences diagnose species boundaries may be the extent to which the mt chromosomes engage in recombination.

 
more » « less
Award ID(s):
1754152
NSF-PAR ID:
10442910
Author(s) / Creator(s):
 
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
10
Issue:
17
ISSN:
2045-7758
Page Range / eLocation ID:
p. 9048-9059
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Background

    Most, if not all, green plant (Virdiplantae) species including angiosperms and ferns are polyploids themselves or have ancient polyploid or whole genome duplication signatures in their genomes. Polyploids are not only restricted to our major crop species such as wheat, maize, potato and the brassicas, but also occur frequently in wild species and natural habitats. Polyploidy has thus been viewed as a major driver in evolution, and its influence on genome and chromosome evolution has been at the centre of many investigations. Mechanistic models of the newly structured genomes are being developed that incorporate aspects of sequence evolution or turnover (low-copy genes and regulatory sequences, as well as repetitive DNAs), modification of gene functions, the re-establishment of control of genes with multiple copies, and often meiotic chromosome pairing, recombination and restoration of fertility.

    Scope

    World-wide interest in how green plants have evolved under different conditions – whether in small, isolated populations, or globally – suggests that gaining further insight into the contribution of polyploidy to plant speciation and adaptation to environmental changes is greatly needed. Forward-looking research and modelling, based on cytogenetics, expression studies, and genomics or genome sequencing analyses, discussed in this Special Issue of the Annals of Botany, consider how new polyploids behave and the pathways available for genome evolution. They address fundamental questions about the advantages and disadvantages of polyploidy, the consequences for evolution and speciation, and applied questions regarding the spread of polyploids in the environment and challenges in breeding and exploitation of wild relatives through introgression or resynthesis of polyploids.

    Conclusion

    Chromosome number, genome size, repetitive DNA sequences, genes and regulatory sequences and their expression evolve following polyploidy – generating diversity and possible novel traits and enabling species diversification. There is the potential for ever more polyploids in natural, managed and disturbed environments under changing climates and new stresses.

     
    more » « less
  2. The ciliate genus Paramecium served as one of the first model systems in microbial eukaryotic genetics, contributing much to the early understanding of phenomena as diverse as genome rearrangement, cryptic speciation, cytoplasmic inheritance, and endosymbiosis, as well as more recently to the evolution of mating types, introns, and roles of small RNAs in DNA processing. Substantial progress has recently been made in the area of comparative and population genomics. Paramecium species combine some of the lowest known mutation rates with some of the largest known effective populations, along with likely very high recombination rates, thereby harboring a population-genetic environment that promotes an exceptionally efficient capacity for selection. As a consequence, the genomes are extraordinarily streamlined, with very small intergenic regions combined with small numbers of tiny introns. The subject of the bulk of Paramecium research, the ancient Paramecium aurelia species complex, is descended from two whole-genome duplication events that retain high degrees of synteny, thereby providing an exceptional platform for studying the fates of duplicate genes. Despite having a common ancestor dating to several hundred million years ago, the known descendant species are morphologically indistinguishable, raising significant questions about the common view that gene duplications lead to the origins of evolutionary novelties.

     
    more » « less
  3. Abstract

    Many applications in molecular ecology require the ability to match specific DNA sequences from single‐ or mixed‐species samples with a diagnostic reference library. Widely used methods for DNA barcoding and metabarcoding employ PCR and amplicon sequencing to identify taxa based on target sequences, but the target‐specific enrichment capabilities of CRISPR‐Cas systems may offer advantages in some applications. We identified 54,837 CRISPR‐Cas guide RNAs that may be useful for enriching chloroplast DNA across phylogenetically diverse plant species. We tested a subset of 17 guide RNAs in vitro to enrich plant DNA strands ranging in size from diagnostic DNA barcodes of 1,428 bp to entire chloroplast genomes of 121,284 bp. We used an Oxford Nanopore sequencer to evaluate sequencing success based on both single‐ and mixed‐species samples, which yielded mean chloroplast sequence lengths of 2,530–11,367 bp, depending on the experiment. In comparison to mixed‐species experiments, single‐species experiments yielded more on‐target sequence reads and greater mean pairwise identity between contigs and the plant species' reference genomes. But nevertheless, these mixed‐species experiments yielded sufficient data to provide ≥48‐fold increase in sequence length and better estimates of relative abundance for a commercially prepared mixture of plant species compared to DNA metabarcoding based on the chloroplasttrnL‐P6 marker. Prior work developed CRISPR‐based enrichment protocols for long‐read sequencing and our experiments pioneered its use for plant DNA barcoding and chloroplast assemblies that may have advantages over workflows that require PCR and short‐read sequencing. Future work would benefit from continuing to develop in vitro and in silico methods for CRISPR‐based analyses of mixed‐species samples, especially when the appropriate reference genomes for contig assembly cannot be known a priori.

     
    more » « less
  4. SUMMARY

    Plant nuclear genomes harbor sequence elements derived from the organelles (mitochondrion and plastid) through intracellular gene transfer (IGT). Nuclear genomes also show a dramatic range of repeat content, suggesting that any sequence can be readily amplified. These two aspects of plant nuclear genomes are well recognized but have rarely been linked. Through investigation of 31Medicagotaxa we detected exceptionally high post‐IGT amplification of mitochondrial (mt) DNA sequences containingrps10in the nuclear genome ofMedicago polymorphaand closely related species. The amplified sequences were characterized as tandem arrays of five distinct repeat motifs (2157, 1064, 987, 971, and 587 bp) that have diverged from the mt genome (mitogenome) in theM. polymorphanuclear genome. The mtrps10‐like arrays were identified in seven loci (six intergenic and one telomeric) of the nuclear chromosome assemblies and were the most abundant tandem repeat family, representing 1.6–3.0% of total genomic DNA, a value approximately three‐fold greater than the entire mitogenome inM. polymorpha. Compared to a typical mt gene, the mtrps10‐like sequence coverage level was 691.5–7198‐fold higher inM. polymorphaand closely related species. In addition to the post‐IGT amplification, our analysis identified the canonical telomeric repeat and the species‐specific satellite arrays that are likely attributable to an ancestral chromosomal fusion inM. polymorpha. A possible relationship between chromosomal instability and the mtrps10‐like tandem repeat family in theM. polymorphaclade is discussed.

     
    more » « less
  5. ABSTRACT

    Psocodea (booklice and parasitic lice) is an order of insects containing species with extensive mitochondrial genome rearrangements, particularly within the suborder Troctomorpha, in which some species possess an extremely fragmented mitochondrial genome with several small minichromosomes. In the remaining suborders of Psocodea, there are groups with the ancestral pancrustacean arrangement, quite extensive rearrangements (e.g. Trogiomorpha), or in which the small number of species analysed to date have rearrangements of only a few protein‐coding genes and/or tRNAs (e.g. Psocomorpha). Despite the apparent high rate of rearrangements in the order as a whole, a small number of complete mitochondrial genomes are available, especially for suborder Psocomorpha, the largest free‐living suborder. To understand the evolution of the gene arrangement of the mitochondrial genome within Psocomorpha and its phylogenetic implications, we assembled and analysed the mitochondrial genomes of 33 species of bark lice belonging to nine families in two infraorders. Within the infraorder Homilopsocidea, four families were analysed, mainly from Lachesillidae (which included 22 species of this family). Within the infraorder Caeciliusetae, seven species representing five families were analysed. Mitochondrial gene rearrangements were identified in seven of the nine families. Some of these rearrangements were unique to a single species, while some contained phylogenetic signal, being shared by related species. These rearrangements typically corresponded to transpositions and inversions of tRNAs, possibly caused by tandem duplication–random loss (TDRL) and/or recombination events. Phylogenetic analyses of mitochondrial gene sequences provided phylogenetic resolution for several branches of the tree, including monophyly of Lachesillinae. The genusHemicaeciliusEnderlein was found to be embedded within the genusLachesillaWestwood, rending the latter paraphyletic. Monophyly was also never recovered for Lachesillidae and Elipsocidae as currently defined. However, instability was observed for some higher level relationships within Psocomorpha, including the relationships among the major clades of Lachesillidae.

     
    more » « less