Butterfly genomics sheds light on the process of hybrid speciation

How common is hybridization between species and what effect does it have on the evolutionary process? Can hybridization generate new species and what indeed is a species? In this issue, Gompert et al. (2014) show how massive, genome‐scale data sets can be used to shed light on these questions. They focus on the Lycaeides butterflies, and in particular, several populations from the western USA, which have characteristics suggesting that they may contain hybrids of two or more different species (Gompert et al. 2006). They demonstrate that these populations do contain mosaic genomes made up of components from different parental species. However, this appears to have been largely driven by historical admixture, with more recent processes appearing to be isolating the populations from each other. Therefore, these populations are on their way to becoming distinct species (if they are not already) but have arisen following extensive hybridization between other distinct populations or species (Fig.  1 ).

Figure 1 Open in figure viewer PowerPoint There has been extensive historical admixture between Lycaeides species with some new species arising from hybrid populations. (Photo credits: Lauren Lucas, Chris Nice, and James Fordyce).

Their data set must be one of the largest outside of humans, with over one and half thousand butterflies genotyped at over 45 thousand variable nucleotide positions. It is this sheer amount of data that has allowed the researchers to distinguish between historical and more recent evolutionary and demographic processes. This is because it has allowed them to partition the data into common and rare genetic variants and perform separate analyses on these. Common genetic variants are likely to be older while rare variants are more likely to be due to recent mutations. Therefore, by splitting the genetic variation into these components, the researchers were able to show more admixture among common variants, while rare variants showed less admixture and clear separation of the populations. The extensive geographic sampling of individuals, including overlapping distributions of several of the putative species, also allowed the authors to rule out the possibility that the separation of the populations was simply due to geographical distance. The authors have developed a new programme for detecting population structure and admixture, which does the same job as STRUCTURE (Pritchard et al. 2000 ), identifying genetically distinct populations and admixture between these populations, but is designed to be used with next generation sequence data. They use the output of this model for another promising new method to distinguish between contemporary and historical admixtures. They fixed the number of source populations in the model at two and estimated the proportion of each individual's genome coming from these two populations. Therefore, an individual can either be purely population 1, or population 2 or some mixture of the two (they call this value q, the same parameter exists in STRUCTURE). They then compared this to the level of heterozygosity coming from the two source populations in the individual's genome. If an individual is an F1 hybrid of two source populations, then it would have a q of 0.5 and also be heterozygous at all loci that distinguish the parental populations. On the other hand, if it is a member of a stable hybrid lineage, it might also have a q of 0.5 but would not be expected to be heterozygous at these loci, because over time the population would become fixed for one or other of the source population states either by drift or selection (Fig.  2 ). This is indeed what they find in the hybrid populations. They tend to have intermediate q values, but the level of heterozygosity coming from the source populations (which they call Q₁₂) was consistently lower than expected.

Figure 2 Open in figure viewer PowerPoint The Q‐matrix analysis used by Gompert et al. ( 2014 ) to distinguish between contemporary (hybrid swarm) and historical (stable hybrid lineage) admixture.

Overall, the results support several of the populations as being stable hybrid lineages. Nevertheless, the strictest definitions of hybrid species specify that the process of hybridization between the parental species must be instrumental in driving the reproductive isolation of the new species from both parental populations (Abbott et al. 2013 ). This is extremely hard to demonstrate conclusively because it requires us to first of all identify the isolating mechanisms that operated in the early evolution of the species and then to show that these were caused by the hybridization event itself. One advantage of the Lycaeides system is that the species appear to be in the early stages of divergence, so barriers to gene flow that are operating currently are likely to be those that are driving the species divergence. While there is some evidence that hybridization gave rise to traits that allowed the new populations to colonize new environments (Gompert et al. 2006 ; Lucas et al. 2008 ), there is clearly further work to be carried out in this direction. One of the rare examples of homoploid hybrid speciation (hybrid speciation without a change in chromosome number) where the reproductive isolation criterion has been demonstrated, comes from the Heliconius butterflies. In this case, hybridization of two species has been shown to give rise to a new colour pattern that instantly becomes reproductively isolated from the parental species due to mate preference for that pattern (Mavárez et al. 2006 ). However, while this has become a widely accepted example (Abbott et al. 2013 ), the naturally occurring ‘hybrid species’ in fact has derived most of its genome from one of the parental species, with largely just the colour pattern controlling locus coming from the other parent, a process that has been termed ‘hybrid trait speciation’ (Salazar et al. 2010 ). This distinction is an important one in terms of our understanding of the organization of biological diversity. While hybrid trait speciation will still largely fit the model of a neatly branching evolutionary tree, with perhaps only the region surrounding the single introgressed gene deviating from this model, hybrid species that end up with mosaic genomes, like Lycaeides, will not fit this model when considering the genome as a whole. This distinction also more broadly applies when comparing the patterns of divergence between Heliconius and Lycaeides. These two butterfly genera have been driving forward our understanding of the prevalence and importance of hybridization at the genomic level, but they reveal different ways in which hybridization can influence the organization of biological diversity. Recent work in Heliconius has shown that admixture is extensive and has been ongoing over a large portion of the evolutionary history of species (Martin et al. 2013 ; Nadeau et al. 2013 ). Nevertheless, this has not obscured the clear and robust pattern of a bifurcating evolutionary tree when considering the genome as a whole (Nadeau et al. 2013 ). In contrast in Lycaeides, the genome‐wide phylogeny clearly does not fit a bifurcating tree, resembling more of a messy shrub, with hybrid taxa falling at intermediate positions on the phylogeny (Gompert et al. 2014 ). The extent to which we need to rethink the way we describe and organize biological diversity will depend on the relative prevalence of these different outcomes of hybridization. We are likely to see many more of these types of large sequence data sets for ecologically interesting organisms. Gompert et al. ( 2014 ) show that these data need not only be a quantitative advance, but can also qualitatively change our understanding of the evolutionary history of these organisms. In particular, analysing common and rare genetic variants separately may provide information that would otherwise be missed. The emerging field of ‘speciation genomics’ (Seehausen et al. 2014 ) should follow this lead in developing new ways of making the most of the flood of genomic data that is being generated, but also improve methods for integrating this with field observations and experiments to identify the sources and targets of selection and divergence.

References

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This article was written and figures prepared by N.N. except as specified in the text (photo credits).

Citing Literature

Number of times cited according to CrossRef: 4

• V. Alex Sotola, David S. Ruppel, Timothy H. Bonner, Chris C. Nice, Noland H. Martin, Asymmetric introgression between fishes in the Red River basin of Texas is associated with variation in water quality, Ecology and Evolution, 10.1002/ece3.4901, 9 , 4, (2083-2095), (2019). Wiley Online Library
• Matej Bocek, Dominik Kusy, Michal Motyka, Ladislav Bocak, Persistence of multiple patterns and intraspecific polymorphism in multi-species Müllerian communities of net-winged beetles, Frontiers in Zoology, 10.1186/s12983-019-0335-8, 16 , 1, (2019). Crossref
• Nicola J. Nadeau, Takeshi Kawakami, Population Genomics of Speciation and Admixture, , 10.1007/13836_2018_24, (2018). Crossref
• Amanda Roe, Julian Dupuis, Felix Sperling, Molecular Dimensions of Insect Taxonomy in the Genomics Era, Insect Biodiversity, 10.1002/9781118945568, (547-573), (2017). Wiley Online Library

Volume 23 , Issue 18 September 2014

Pages 4441-4443     

Expression of Melocactus glaucescens SERK1 sheds new light on the mechanism of areolar activation in cacti

Plant Cell, Tissue and Organ Culture (PCTOC) - Areolar activation is the most popular in vitro propagation method for cacti. Even though it is relatively simple, few established protocols exist....     

GFP sheds light on the infection process of avocado roots by Rosellinia necatrix

In order to monitor Rosellinia necatrix infection of avocado roots, we generated a plasmid vector (pCPXHY1eGFP) constitutively expressing EGFP and developed a protoplast transformation protocol. Using this protocol, four R. necatrix isolates were efficiently transformed and were shown to stably express EGFP homogeneously while not having any observable effect on pathogenicity. Confocal laser scanning microscopy (CLSM) images of avocado roots infected with the highly virulent isolate CH53-GFP demonstrated that fungal penetration of avocado roots occurs simultaneously at several random sites, but it occurs preferentially in the crown region as well as throughout the lenticels and in the junctions between epidermal cells. Not only were R. necatrix hyphae observed invading the epidermal and cortical root cells, but they were also able to penetrate the primary and secondary xylem. Scanning electron microscopy (SEM) images allowed detailed visualisation of the hyphal network generated by invasion of R. necatrix through the epidermal, cortical and vascular cells, including hyphal anastomosis and branching points. To our knowledge, this is the first report describing the construction of GFP-tagged strains belonging to the genus Rosellinia for monitoring white root rot using CLSM and SEM.     

Mapping the binding site of arginine vasopressin to V1a and V1b vasopressin receptors

Starting from the 2.8-A resolution x-ray structure of bovine rhodopsin, three-dimensional molecular models of the complexes between arginine vasopressin and two receptor subtypes (V1a, V1b) have been built. Amino acid sequence alignment and docking studies suggest that four key residues (1.35, 2.65, 4.61, and 5.35) fine tune the binding of vasopressin and related peptide agonists to both receptor subtypes. To validate these predictions, a series of single or double mutants were engineered at V1a and V1b receptor subtypes and tested for their binding and functional properties. Two negatively charged amino acids at positions 1.35 and 2.65 are key anchoring residues to the Arg8 residue of arginine vasopressin. Moreover, two amino acids (V(4.61) and P(5.35)) delineating a hydrophobic subsite at the human V1b receptor are responsible for the recognition of V1b selective peptide agonists. Last, one of the latter positions (5.35) is hypothesized to explain the pharmacological species differences between rat and human vasopressin receptors for a V1b peptide agonist. Altogether these refined three-dimensional models of V1a and V1b human receptors should enable the identification of further new selective V1a and V1b agonists as pharmacological but also therapeutic tools.     

Structural biology sheds light on the puzzle of genomic ORFans

Genomic ORFans are orphan open reading frames (ORFs) with no significant sequence similarity to other ORFs. ORFans comprise 20-30% of the ORFs of most completely sequenced genomes. Because nothing can be learnt about ORFans via sequence homology, the functions and evolutionary origins of ORFans remain a mystery. Furthermore, because relatively few ORFans have been experimentally characterized, it has been suggested that most ORFans are not likely to correspond to functional, expressed proteins, but rather to spurious ORFs, pseudo-genes or to rapidly evolving proteins with non-essential roles. As a snapshot view of current ORFan structural studies, we searched for ORFans among proteins whose three-dimensional structures have been recently determined. We find that functional and structural studies of ORFans are not as underemphasized as previously suggested. These recently determined structures correspond to ORFans from all Kingdoms of life, and include proteins that have previously been functionally characterized, as well as structural genomics targets of unknown function labeled as "hypothetical proteins". This suggests that many of the ORFans in the databases are likely to correspond to expressed, functional (and even essential) proteins. Furthermore, the recently determined structures include examples of the various types of ORFans, suggesting that the functions and evolutionary origins of ORFans are diverse. Although this survey sheds some light on the ORFan mystery, further experimental studies are required to gain a better understanding of the role and origins of the tens of thousands of ORFans awaiting characterization.     

Mitochondrial analysis sheds light on the origin of hair sheep

A total of 180 mtDNA sequences from hair Caribbean (93), West African (73) and Canarian‐wooled (14) sheep were analysed to shed light on the origin of hair sheep. A comparison of 360 Iberian sheep sequences retrieved from GenBank was performed to assess a possible European origin of the Caribbean hair sheep. These 180 sequences gave 48 different haplotypes (16 in Caribbean sheep). All Caribbean and Canarian‐wooled sequences and 91.8% of the West African samples belonged to haplogroup B. The sheep analysed showed wide haplotypic identity. Caribbean sheep shared roughly two‐thirds of their samples with Canarian‐wooled and West African samples, respectively. Principal component analysis showed that the Caribbean and the Canarian‐wooled sheep clustered together. Additional analyses showed that hair and Iberian sheep had wide genetic identity. It was not possible to ascertain a single Canarian, African or European origin of the Caribbean hair sheep using mtDNA markers only. European, African and Caribbean hair sheep maternal genetic backgrounds likely result from related domestication events.     

Mapping of the second tetracycline binding site on the ribosomal small subunit of E.coli

Tetracycline blocks stable binding of aminoacyl-tRNA to the bacterial ribosomal A-site. Various tetracycline binding sites have been identified in crystals of the 30S ribosomal small subunit of Thermus thermophilus. Here we describe a direct photo- affinity modification of the ribosomal small subunits of Escherichia coli with 7-[³H]-tetracycline. To select for specific interactions, an excess of the 30S subunits over tetracycline has been used. Primer extension analysis of the 16S rRNA revealed two sites of the modifications: C936 and C948. Considering available data on tetracycline interactions with the prokaryotic 30S subunits, including the presented data (E.coli), X-ray data (T.thermophilus) and genetic data (Helicobacter pylori, E.coli), a second high affinity tetracycline binding site is proposed within the 3′-major domain of the 16S rRNA, in addition to the A-site related tetracycline binding site.     

African lungfish genome sheds light on the vertebrate water-to-land transition

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The structure of the bacteriophage PRD1 spike sheds light on the evolution of viral capsid architecture

Comparisons of bacteriophage PRD1 and adenovirus protein structures and virion architectures have been instrumental in unraveling an evolutionary relationship and have led to a proposal of a phylogeny-based virus classification. The structure of the PRD1 spike protein P5 provides further insight into the evolution of viral proteins. The crystallized P5 fragment comprises two structural domains: a globular knob and a fibrous shaft. The head folds into a ten-stranded jelly roll beta barrel, which is structurally related to the tumor necrosis factor (TNF) and the PRD1 coat protein domains. The shaft domain is a structural counterpart to the adenovirus spike shaft. The structural relationships between PRD1, TNF, and adenovirus proteins suggest that the vertex proteins may have originated from an ancestral TNF-like jelly roll coat protein via a combination of gene duplication and deletion.     

Metal binding sheds light on mechanisms of amyloid assembly

β-2 microglobulin (β2m) is the protein responsible for amyloid deposition in Dialysis-Related Amyloidosis (DRA). Aggregation can be induced by various solution conditions including exposure to divalent metal, incubation at acidic pH, and limited proteolysis. Using Cu²⁺ as a trigger, we have trapped, isolated, and crystallized a stable oligomer of β2m that is populated under amyloidogenic solution conditions (Calabrese et al. Nat Struct Mol Biol 2008; 15:965–71). This structure reveals that Cu²⁺-binding is associated with dramatic conformational rearrangements. This has allowed us to postulate a set of structural changes common to all β2m aggregation pathways. Cu²⁺ serves as a potential trigger in other aggregation systems such as Aβ, α-synuclein, and mammalian Prion (PrP). A comparison of Cu²⁺ binding to β2m and PrP reveals common features. Therefore, in addition to providing insight into DRA, induction of structure by Cu²⁺ binding appears to be a recurring structural motif for pathological changes in conformation.Key words: amyloid, protein folding, dialysis-related amyloidosis, copper, β-2 microglobulin, prion     

Ancient DNA sheds light on the ancestry of pre-hispanic Canarian pigs

Background

Canarian Black (CB) pigs belong to an autochthonous and endangered breed, which is spread throughout the Canarian archipelago. It is commonly accepted that they represent a relic of the pig populations that were bred by the Berbers in North Africa over millennia. It is important to note that the geographic isolation of the Canary Islands has preserved this genetic legacy intact from foreign introgressions until the Spanish conquest of the archipelago in the 15^th century. Ten years ago, it was demonstrated that, in CB pigs, the frequency of the Asian A2 cytochrome-b haplogroup reached 73%. The current work aimed at investigating whether this observation is explained by either a recent or an ancient introgression of CB pigs with Far Eastern pigs.

Results

Genetic analyses of 23 ancient samples from pre-hispanic Canarian pigs (420 to 2500 years before present) showed that Near Eastern and Far Eastern genetic signatures were totally absent in the primitive Canarian pre-hispanic pigs. Indeed, the haplotypes detected in these pigs were closely related to those of North African and European wild boars.

Conclusions

Our results demonstrate that the high frequency of the Far Eastern mitochondrial cytochrome B A2 haplotype in modern Canarian Black pigs probably corresponds to a relatively recent introgression with British breeds.

Electronic supplementary material

The online version of this article (doi:10.1186/s12711-015-0115-7) contains supplementary material, which is available to authorized users.     

Mapping the binding site on small ankyrin 1 for obscurin

Small ankyrin 1 (sAnk1), an integral protein of the sarcoplasmic reticulum encoded by the ANK1 gene, binds with nanomolar affinity to the C terminus of obscurin, a giant protein surrounding the contractile apparatus in striated muscle. We used site-directed mutagenesis to characterize the binding site on sAnk1, specifically addressing the role of two putative amphipathic, positively charged helices. We measured binding qualitatively by blot overlay assays and quantitatively by surface plasmon resonance and showed that both positively charged sequences are required for activity. We showed further that substitution of a lysine or arginine with an alanine or glutamate located at the same position along either of the two putative helices has similar inhibitory or stimulatory effects on binding and that the effects of a particular mutation depended on the position of the mutated amino acid in each helix. We modeled the structure of the binding region of sAnk1 by homology with ankyrin repeats of human Notch1, which have a similar pattern of charged and hydrophobic residues. Our modeling suggested that each of the two positively charged sequences forms pairs of amphipathic, anti-parallel alpha-helices flanked by beta-hairpin-like turns. Most of the residues in homologous positions along each helical unit have similar, though not identical, orientations. CD spectroscopy confirmed the alpha-helical content of sAnk1, approximately 33%, predicted by the model. Thus, structural and mutational studies of the binding region on sAnk1 for obscurin suggest that it consists of two ankyrin repeats with very similar structures.     

Ant genomics sheds light on the molecular regulation of social organization

Ants are powerful model systems for the study of cooperation and sociality. In this review, we discuss how recent advances in ant genomics have contributed to our understanding of the evolution and organization of insect societies at the molecular level.     

Ancient mitochondrial DNA from the northern fringe of the Neolithic farming expansion in Europe sheds light on the dispersion process

The European Neolithization process started around 12 000 years ago in the Near East. The introduction of agriculture spread north and west throughout Europe and a key question has been if this was brought about by migrating individuals, by an exchange of ideas or a by a mixture of these. The earliest farming evidence in Scandinavia is found within the Funnel Beaker Culture complex (Trichterbecherkultur, TRB) which represents the northernmost extension of Neolithic farmers in Europe. The TRB coexisted for almost a millennium with hunter–gatherers of the Pitted Ware Cultural complex (PWC). If migration was a substantial part of the Neolithization, even the northerly TRB community would display a closer genetic affinity to other farmer populations than to hunter–gatherer populations. We deep-sequenced the mitochondrial hypervariable region 1 from seven farmers (six TRB and one Battle Axe complex, BAC) and 13 hunter–gatherers (PWC) and authenticated the sequences using postmortem DNA damage patterns. A comparison with 124 previously published sequences from prehistoric Europe shows that the TRB individuals share a close affinity to Central European farmer populations, and that they are distinct from hunter–gatherer groups, including the geographically close and partially contemporary PWC that show a close affinity to the European Mesolithic hunter–gatherers.     

Mutations within the agonist-binding site convert the homomeric alpha1 glycine receptor into a Zn2+-activated chloride channel

The divalent cation Zn2+ has been shown to regulate inhibitory neurotransmission in the mammalian CNS by affecting the activation of the strychnine-sensitive glycine receptor (GlyR). In spinal neurons and cells expressing recombinant GlyRs, low micromolar (<10 microM) concentrations of Zn2+ enhance glycine currents, whereas higher concentrations (>10 microM) have an inhibitory effect. Mutational studies have localized the Zn2+ binding sites mediating allosteric potentiation and inhibition of GlyRs in distinct regions of the N-terminal extracellular domain of the GlyR alpha-subunits. Here, we examined the Zn2+ sensitivity of different mutations within the agonist binding site of the homomeric alpha(1)-subunit GlyR upon heterologous expression in Xenopus oocytes. This revealed that six substitutions within the ligand-binding pocket result in a total loss of Zn2+ inhibition. Furthermore, substitution of the positively charged residues arginine 65 and arginine 131 by alanine (alpha(1)(R65A), alpha(1)(R131A), or of the aromatic residue phenylalanine 207 by histidine (alpha(1)(F207H)), converted the alpha(1) GlyR into a chloride channel that was activated by Zn2+ alone. Dose-response analysis of the alpha(1)(F207H) GlyR disclosed an EC(50) value of 1.2 microM for Zn2+ activation; concomitantly the apparent glycine affinity was 1000-fold reduced. Thus, single point mutations within the agonist-binding site of the alpha(1) subunit convert the inhibitory GlyR from a glycine-gated into a selectively Zn2+-activated chloride channel. This might be exploited for the design of metal-specific biosensors by modeling-assisted mutagenesis.