Go forth,evolve and prosper: the genetic basis of adaptive evolution in an invasive species

Invasive species stand accused of a familiar litany of offences, including displacing native species, disrupting ecological processes and causing billions of dollars in ecological damage (Cox 1999 ). Despite these transgressions, invasive species have at least one redeeming virtue – they offer us an unparalleled opportunity to investigate colonization and responses of populations to novel conditions in the invaded habitat (Elton 1958 ; Sakai et al. 2001 ). Invasive species are by definition colonists that have arrived and thrived in a new location. How they are able to thrive is of great interest, especially considering a paradox of invasion (Sax & Brown 2000 ): if many populations are locally adapted (Leimu & Fischer 2008 ), how could species introduced into new locations become so successful? One possibility is that populations adjust to the new conditions through plasticity – increasing production of allelopathic compounds (novel weapons), or taking advantage of new prey, for example. Alternatively, evolution could play a role, with the populations adapting to the novel conditions of the new habitat. There is increasing evidence, based on phenotypic data, for rapid adaptive evolution in invasive species (Franks et al. 2012 ; Colautti & Barrett 2013 ; Sultan et al. 2013 ). Prior studies have also demonstrated genetic changes in introduced populations using neutral markers, which generally do not provide information on adaptation. Thus, the genetic basis of adaptive evolution in invasive species has largely remained unknown. In this issue of Molecular Ecology, Vandepitte et al. ( 2014 ) provide some of the first evidence in invasive populations for molecular genetic changes directly linked to adaptation.     

Pathogen pollution and the emergence of a deadly amphibian pathogen

Imagine a single pathogen that is responsible for mass mortality of over a third of an entire vertebrate class. For example, if a single pathogen were causing the death, decline and extinction of 30% of mammal species (including humans), the entire world would be paying attention. This is what has been happening to the world's amphibians – the frogs, toads and salamanders that are affected by the chytrid fungal pathogen, Batrachochytrium dendrobatidis (referred to as Bd), which are consequently declining at an alarming rate. It has aptly been described as the worst pathogen in history in terms of its effects on biodiversity (Kilpatrick et al. 2010). The pathogen was only formally described about 13 years ago (Longcore et al. 1999), and scientists are still in the process of determining where it came from and investigating the question: why now? Healthy debate has ensued as to whether Bd is a globally endemic organism that only recently started causing high mortality due to shifting host responses and/or environmental change (e.g. Pounds et al. 2006) or whether a virulent strain of the pathogen has rapidly disseminated around the world in recent decades, affecting new regions with a vengeance (e.g. Morehouse et al. 2003; Weldon et al. 2004; Lips et al. 2008). We are finally beginning to shed more light on this question, due to significant discoveries that have emerged as a result of intensive DNA‐sequencing methods comparing Bd isolates from different amphibian species across the globe. Evidence is mounting that there is indeed a global panzootic lineage of Bd (BdGPL) in addition to what appear to be more localized endemic strains (Fisher et al. 2009; James et al. 2009; Farrer et al. 2011). Additionally, BdGPL appears to be a hypervirulent strain that has resulted from the hybridization of different Bd strains that came into contact in recent decades, and is now potentially replacing the less‐virulent endemic strains of the pathogen (Farrer et al. 2011). In a new study published in this issue of Molecular Ecology, Schloegel et al. (2012) identify an additional unique Bd lineage that is endemic to the Atlantic Brazilian rainforests (Bd‐Brazil) and provide striking evidence that the Bd‐Brazil lineage has sexually recombined with the BdGPL lineage in an area where the two lineages likely came into contact as a result of classic anthropogenically mediated ‘pathogen pollution’(see below). Fungal pathogens, including Bd, have the propensity to form recombinant lineages when allopatric populations that have not yet formed genetic reproductive barriers are provided with opportunities to intermingle, and virulent strains may be selected for because they tend to be highly transmissible (Fisher et al. 2012). As Schloegel et al. (2012) point out, the demonstrated ability for Bd to undergo meiosis may also mean that it has the capacity to form a resistant spore stage (as yet undiscovered), based on extrapolation from other sexually reproducing chytrids that all have spore stages.     

Population genomics and the causes of local differentiation

Exactly 50 years ago, a revolution in empirical population genetics began with the introduction of methods for detecting allelic variation using protein electrophoresis (Throckmorton 1962; Hubby 1963; Lewontin & Hubby 1966). These pioneering scientists showed that populations are chock‐full of genetic variation. This variation was a surprise that required a re‐thinking of evolutionary genetic heuristics. Understanding the causes for the maintenance of this variation became and remains a major area of research. In the process of addressing the causes, this same group of scientists documented geographical genetic structure (Prakash et al. 1969), spawning the continued accumulation of what is now a huge case study catalogue of geographical differentiation (e.g. Loveless & Hamrick 1984; Linhart & Grant 1996). Geographical differentiation is clearly quite common. Yet, a truly general understanding of the patterns in and causes of spatial genetic structure across the genome remains elusive. To what extent is spatial structure driven by drift and phylogeography vs. geographical differences in environmental sources of selection? What proportion of the genome participates? A general understanding requires range‐wide data on spatial patterning of variation across the entire genome. In this issue of Molecular Ecology, Lasky et al. (2012) make important strides towards addressing these issues, taking advantage of three contemporary revolutions in evolutionary biology. Two are technological: high‐throughput sequencing and burgeoning computational power. One is cultural: open access to data from the community of scientists and especially data sets that result from large collaborative efforts. Together, these developments may at last put answers within reach.     

Genomics of clinal variation in Drosophila: disentangling the interactions of selection and demography

Clines in phenotypes and genotype frequencies across environmental gradients are commonly taken as evidence for spatially varying selection. Classical examples include the latitudinal clines in various species of Drosophila, which often occur in parallel fashion on multiple continents. Today, genomewide analysis of such clinal systems provides a fantastic opportunity for unravelling the genetics of adaptation, yet major challenges remain. A well‐known but often neglected problem is that demographic processes can also generate clinality, independent of or coincident with selection. A closely related issue is how to identify true genic targets of clinal selection. In this issue of Molecular Ecology, three studies illustrate these challenges and how they might be met. Bergland et al. report evidence suggesting that the well‐known parallel latitudinal clines in North American and Australian D. melanogaster are confounded by admixture from Africa and Europe, highlighting the importance of distinguishing demographic from adaptive clines. In a companion study, Machado et al. provide the first genomic comparison of latitudinal differentiation in D. melanogaster and its sister species D. simulans. While D. simulans is less clinal than D. melanogaster, a significant fraction of clinal genes is shared between both species, suggesting the existence of convergent adaptation to clinaly varying selection pressures. Finally, by drawing on several independent sources of evidence, Bo?i?evi? et al. identify a functional network of eight clinal genes that are likely involved in cold adaptation. Together, these studies remind us that clinality does not necessarily imply selection and that separating adaptive signal from demographic noise requires great effort and care.     

A closer look at the spatial architecture of aphid clones

Nearly 25 years ago, Ellstrand & Roose (1987) reviewed what was known at the time of the genetic structure of clonal plant species. What is the relationship between space and clonal fitness, they asked. What is the best way for a clone to grow within its ecological neighbourhood? The pot had been stirred 10 years previously by Janzen (1977) , who pointed out how little we know about the population biology of clonal organisms like dandelions and aphids. He wondered whether, like good curries, outward appearances masked common ingredients. Because in no small part of the advent of molecular ecology, we know more about clonal life histories today, particularly in plants ( van Dijk 2003 ; Vallejo‐Marín et al. 2010 ). Surprisingly, studies of the spatial architecture of aphid clones have been comparably rare. In this issue of Molecular Ecology, Vantaux et al. characterize the fine‐scale distribution of the black bean aphid (Aphis fabae) and in so doing, help to fill that gap. They describe a moderate degree of intermingling between aphid clones over a growing season—A. fabae clones are ‘sticky’, but only a bit. By mixing, clones directly compete with each other as well. The results of Vantaux et al. (2011) will help to integrate evolutionary patterns in aphids with the appropriate ecological scales out of which those patterns emerge.     

Phenotypic plasticity and divergence in gene expression

The extent to which phenotypic plasticity, or the ability of a single genotype to produce different phenotypes in different environments, impedes or promotes genetic divergence has been a matter of debate within evolutionary biology for many decades (see, for example, Ghalambor et al. 2007 ; Pfennig et al. 2010 ). Similarly, the role of evolution in shaping phenotypic plasticity remains poorly understood (Pigliucci 2005 ). In this issue of Molecular Ecology, Dayan et al. ( 2015 ) provide empirical data relevant to these questions by assessing the extent of plasticity and divergence in the expression levels of 2272 genes in muscle tissue from killifish (genus Fundulus) exposed to different temperatures. F. heteroclitus (Fig.  1 A) and F. grandis are minnows that inhabit estuarine marshes (Fig.  1 B) along the coasts of the Atlantic Ocean and Gulf of Mexico in North America. These habitats undergo large variations in temperature both daily and seasonally, and these fish are known to demonstrate substantial phenotypic plasticity in response to temperature change (e.g. Fangue et al. 2006 ). Furthermore, the range of F. heteroclitus spans a large latitudinal gradient of temperatures, such that northern populations experience temperatures that are on average ~10°C colder than do southern populations (Schulte 2007 ). By comparing gene expression patterns between populations of these fish from different thermal habitats held in the laboratory at three different temperatures, Dayan et al. ( 2015 ) address two important questions regarding the interacting effects of plasticity and evolution: (i) How does phenotypic plasticity affect adaptive divergence? and (ii) How does adaptive divergence affect plasticity?     

The relative lengths of individual telomeres are defined in the zygote and strictly maintained during life

Previous studies have indicated that average telomere length is partly inherited ( Slagboom et al., 1994 ; Rufer et al., 1999 ) and that there is an inherited telomere pattern in each cell ( Graakjaer et al., 2003 ); ( Londoño‐Vallejo et al., 2001 ). In this study, we quantify the importance of the initially inherited telomere lengths within cells, in relation to other factors that influence telomere length during life. We have estimated the inheritance by measuring telomere length in monozygotic (MZ) twins using Q‐FISH with a telomere specific peptide nucleic acid (PNA)‐probe. Homologous chromosomes were identified using subtelomeric polymorphic markers. We found that identical homologous telomeres from two aged MZ twins show significantly less differences in relative telomere length than when comparing the two homologues within one individual. This result means that towards the end of life, individual telomeres retain the characteristic relative length they had at the outset of life and that any length alteration during the lifespan impacts equally on genetically identical homologues. As the result applies across independent individuals, we conclude that, at least in lymphocytes, epigenetic/environmental effects on relative telomere length are relatively minor during life.     

Tracing the recombination and colonization history of hybrid species in space and time

Hybrid speciation has long fascinated evolutionary biologists and laymen alike, presumably because it challenges our classical view of evolution as a ‘one‐way street’ leading to strictly tree‐like patterns of ancestry and descent. Homoploid hybrid speciation (HHS) has been a particularly interesting puzzle, as it appears to occur extremely rapidly, perhaps within less than 50 generations ( McCarthy et al. 1995 ; Buerkle et al. 2000 ). Nevertheless, HHS may sometimes involve extended or repeated periods of recombination and gene exchange between populations subject to strong divergent natural selection ( Buerkle & Rieseberg 2008 ). Thus, HHS provides a highly interesting setting for understanding the drivers and tempo of adaptive divergence and speciation in the face of gene flow ( Arnold 2006 ; Rieseberg & Willis 2007 ; Nolte & Tautz 2009). In the present issue of Molecular Ecology, Wang et al. (2011) explore a particularly challenging issue connected to HHS: they attempt to trace the colonization and recombination history of an ancient (several MYA) hybrid species, from admixture and recombination in the ancestral hybrid zone to subsequent range shifts triggered by tectonic events (uplift of the Tibetan plateau) and climatic shifts (Pleistocene ice ages). This work is important because it addresses key issues related to the origin of the standing genetic variation available for adaptive responses (e.g. to climate change) and speciation in temperate species, which are topics of great current interest ( Rieseberg et al. 2003 ; Barrett & Schluter 2008 ; de Carvalho et al. 2010 ).     

Fission and fusion in island taxa – serendipity,or something to be expected?

A well‐used metaphor for oceanic islands is that they act as ‘natural laboratories’ for the study of evolution. But how can islands or archipelagos be considered analogues of laboratories for understanding the evolutionary process itself? It is not necessarily the case that just because two or more related species occur on an island or archipelago, somehow, this can help us understand more about their evolutionary history. But in some cases, it can. In this issue of Molecular Ecology, Garrick et al. ( 2014 ) use population‐level sampling within closely related taxa of Galapagos giant tortoises to reveal a complex demographic history of the species Chelonoidis becki – a species endemic to Isabela Island, and geographically restricted to Wolf Volcano. Using microsatellite genotyping and mitochondrial DNA sequencing, they provide a strong case for C. becki being derived from C. darwini from the neighbouring island of Santiago. But the interest here is that colonization did not happen only once. Garrick et al. ( 2014 ) reveal C. becki to be the product of a double colonization event, and their data reveal these two founding lineages to be now fusing back into one. Their results are compelling and add to a limited literature describing the evolutionary consequences of double colonization events. Here, we look at the broader implications of the findings of Garrick et al. ( 2014 ) and suggest genomic admixture among multiple founding populations may be a characteristic feature within insular taxa.     

Next‐generation QTL mapping: crowdsourcing SNPs,without pedigrees

For many molecular ecologists, the mantra and mission of the field of ecological genomics could be encapsulated by the phrase ‘to find the genes that matter’ (Mitchell‐Olds 2001 ; Rockman 2012 ). This phrase of course refers to the early hope and current increasing success in the search for genes whose variation underlies phenotypic variation and fitness in natural populations. In the years since the modern incarnation of the field of ecological genomics, many would agree that the low‐hanging fruit has, at least in principle, been plucked: we now have several elegant examples of genes whose variation influences key adaptive traits in natural populations, and these examples have revealed important insights into the architecture of adaptive variation (Hoekstra et al. 2006 ; Shapiro et al. 2009 ; Chan et al. 2010 ). But how well will these early examples, often involving single genes of large effect on discrete or near‐discrete phenotypes, represent the dynamics of adaptive change for the totality of phenotypes in nature? Will traits exhibiting continuous rather than discrete variation in natural populations have as simple a genetic basis as these early examples suggest (Prasad et al. 2012 ; Rockman 2012 )? Two papers in this issue (Robinson et al. 2013 ; Santure et al. 2013 ) not only suggest answers to these questions but also provide useful extensions of statistical approaches for ecological geneticists to study the genetics of continuous variation in nature. Together these papers, by the same research groups studying evolution in a natural population of Great Tits (Parus major), provide a glimpse of what we should expect as the field begins to dissect the genetic basis of what is arguably the most common type of variation in nature, and how genome‐wide surveys of variation can be applied to natural populations without pedigrees.     

Ring species as demonstrations of the continuum of species formation

In the mid‐20th century, Ernst Mayr (1942) and Theodosius Dobzhansky (1958) championed the significance of ‘circular overlaps’ or ‘ring species’ as the perfect demonstration of the gradual nature of species formation. As an ancestral species expands its range, wrapping around a geographic barrier, derived taxa within the ring display interactions typical of populations, such as genetic and morphological intergradation, while overlapping taxa at the terminus of the ring behave largely as sympatric, reproductively isolated species. Are ring species extremely rare or are they just difficult to detect? What conditions favour their formation? Modelling studies have attempted to address these knowledge gaps by estimating the biological parameters that result in stable ring species (Martins et al. 2013), and determining the necessary topographic parameters of the barriers encircled (Monahan et al. 2012). However, any generalization is undermined by a major limitation: only a handful of ring species are known to exist in nature. In addition, many of them have been broken into multiple species presumed to be evolving independently, usually obscuring the evolutionary dynamics that generate diversity. A paper in this issue of Molecular Ecology by Fuchs et al. (2015), focused on the entire genealogy of a bulbul (Alophoixus) species complex, offers key insights into the evolutionary processes underlying diversification of this Indo‐Malayan bird. Their findings fulfil most of the criteria that can be expected for ring species (Fig.  1 ): an ancestor has colonized the mainland from Sundaland, expanded along the forested habitat wrapping around Thailand's lowlands, adjacent taxa intergrade around the ring distribution, and terminal taxa overlap at the ring closure. Although it remains unclear whether ring divergence has resulted in restrictive gene flow relative to that observed around the ring, their results suggest that circular overlaps might be more common in nature than currently recognized in the literature. Most importantly, this work shows that the continuum of species formation that Mayr and Dobzhansky praised in circular overlaps is found in biological systems currently described as ‘rings of species’, in addition to the idealized ‘ring species’.     

Towards natural polyploid model organisms

Populations of natural allopolyploids with available and well‐developed genomic resources are currently hard to come by. These are needed because whole genome duplication and hybridization — both combined in allopolyploids — are significant processes in evolution, especially the evolution of plants. The new characterization of a naturally occurring allopolyploid in the genus Mimulus by Sweigart et al. in this issue of Molecular Ecology is therefore to be welcomed. Mimulus is rapidly emerging as a model system for evolutionary functional genomics. Sequences of the whole genome and 200 000 expressed sequence tags of diploid M. guttatus, a putative parent of the polyploid described in this issue, will soon be available. These will facilitate investigation of the fates of genes duplicated by whole genome duplication, and their effects on morphology, mating system and ecology in natural populations.     

铬黄圆痕叶蝉属的订正及圆痕叶蝉族巴西二新属二新种描记（半翅目：叶蝉科）

基于比较形态学对曾归入圆痕叶蝉亚科铬黄圆痕叶蝉属Chromagallia的8个有效种（C. saucia (St?l), C. flavofasciata (St?l), C. longistilata (Coelho & Dutra), C. carvalhoi Gon?alves et al., C. lamasi Gon?alves et al., C. lanceolata Gon?alves et al., C. paraguayensis Gon?alves et al.和C. zanolae Gon?alves et al.）进行了订正,明确了该属的范围仅限于具有黄斑的3个种（C. flavofasciata (St?l), C. longistilata (Coelho & Dutra) 和C. rodriguesoi sp. nov.）,对该属进行了重新描述,并修订了鉴别特征。此外,对模式种C. flavofasciata 进行了重新描记,首次提供了C. longistilata的雌性生殖器图,并作了描记。把曾归入铬黄圆痕叶蝉属Chromagallia具有红斑的6个种移出并新建了2个新属：Rubragallia 和Neorubragallia,其中Rubragallia 包括R. saucia (St?l) n. comb.和R. paraguayensis (Gon?alves et al.) n. comb., Neorubragallia包括N. lamasi (Gon?alves et al.) n. comb., N. lanceolata (Gon?alves et al.) n. comb., N. zanolae (Gon?alves et al.) n. comb., N. carvalhoi (Gon?alves et al.) n. comb. 和N. mervini sp. nov.。文中提供了3个属的分种检索表,并对不同种的分类地位及3个属的划分进行了讨论。     

A sea water barrier to coral gene flow

Land is not the only barrier to dispersal encountered by marine organisms. For sedentary shallow water species, there is an additional, marine barrier, 5000 km of uninterrupted deep‐water stretch between the central and the eastern Pacific. This expanse of water, known as the ‘Eastern Pacific Barrier’, has been separating faunas of the two oceanic regions since the beginning of the Cenozoic. Species with larvae that cannot stay in the plankton for the time it takes to cross between the two sides have been evolving independently. That the eastern Pacific does not share species with the rest of the Pacific was obvious to naturalists two centuries ago (Darwin 1860). Yet, this rule has exceptions. A small minority of species are known to straddle the Eastern Pacific Barrier. One such exception is the scleractinian coral Porites lobata (Fig.  1 ). This species is spread widely throughout the Indo‐Pacific, where it is one of the major reef‐builders, but it is also encountered in the eastern Pacific. Are eastern and central Pacific populations of this coral connected by gene flow? In this issue of Molecular Ecology, Baums et al. (2012) use microsatellite data to answer this question. They show that P. lobata populations in the eastern Pacific are cut off from genetic influx from the rest of the Pacific. Populations within each of the two oceanic regions are genetically connected (though those in the Hawaiian islands are also isolated). Significantly, the population in the Clipperton Atoll, the westernmost island in the eastern Pacific, genetically groups with populations from the central Pacific, suggesting that crossing the Eastern Pacific Barrier by P. lobata propagules does occasionally occur.     

Speciation genetics of biological invasions with hybridization

The negative effects of human‐induced habitat disturbance and modification on multiple dimensions of biological diversity are well chronicled ( Turner 1996 ; Harding et al. 1998 ; Lawton et al. 1998 ; Sakai et al. 2001 ). Among the more insidious consequences is secondary contact between formerly allopatric taxa ( Anderson & Hubricht 1938 ; Perry et al. 2002 ; Seehausen 2006 ). How the secondary contact will play out is unpredictable ( Ellstrand et al. 2010 ), but if the taxa are not fully reproductively isolated, hybridization is likely, and if the resulting progeny are fertile, the eventual outcome is often devastating from a conservation perspective ( Rhymer & Simberloff 1996 ; Wolf et al. 2001 ; McDonald et al. 2008 ). In this issue of Molecular Ecology, Steeves et al. (2010) present an analysis of hybridization between two avian species, one of which is critically endangered and the other of which is invasive. Their discovery that the endangered species has not yet been hybridized to extinction is promising and not what one would necessarily expect from theory.     

Reanalysis of the biogeographical hypothesis of range expansion between robust and gracile capuchin monkeys

The data used by Lynch Alfaro et al. (2012a, Journal of Biogeography, 39 , 272–288) and the biogeographical hypothesis postulated by these authors to explain the current distribution of capuchin monkeys were reanalysed including additional cytochrome b data from Sapajus xanthosternos and Sapajus flavius. Our reconstructed phylogeny placed S. xanthosternos in a monophyletic clade representing the most basal lineage of this genus. All analyses indicated polyphyletic arrangements for several capuchin species, suggesting that incomplete lineage sorting has occurred during their evolution. These results also suggest that available molecular data lack adequate variation for accurately resolving species relationships. These results suggest that the divergence of capuchin monkey genera may have occurred in the Atlantic Forest. However, a more conclusive scenario and better resolution of the species tree requires correct identification of species, data from several unlinked nuclear loci from a higher number of individuals per species, and careful analysis of ancient DNA data from museum specimens.     

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.

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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     

Within-genotype epigenetic variation enables broad niche width in a flower living yeast

Niche theory is one of the central organizing concepts in ecology. Generally, this theory defines a given species niche as all of the factors that effect the persistence of the species as well as the impact of the species in a given location ( Hutchinson 1957 ; Chase 2011 ). Many studies have argued that phenotypic plasticity enhances niche width because plastic responses allow organisms to express advantageous phenotypes in a broader range of environments ( Bradshaw 1965 ; Van Valen 1965 ; Sultan 2001 ). Further, species that exploit habitats with fine‐grained variation, or that form metapopulations, are expected to develop broad niche widths through phenotypic plasticity ( Sultan & Spencer 2002 ; Baythavong 2011 ). Although a long history of laboratory, greenhouse and reciprocal transplant experiments have provided insight into how plasticity contributes to niche width ( Pigliucci 2001 ), recent advances in molecular approaches allow for a mechanistic understanding of plasticity at the molecular level ( Nicotra et al. 2010 ). In particular, variation in epigenetic effects is a potential source of the within‐genotype variation that underlies the phenotypic plasticity associated with broad niche widths. Epigenetic mechanisms can alter gene expression and function without altering DNA sequence ( Richards 2006 ) and may be stably transmitted across generations ( Jablonka & Raz 2009 ; Verhoeven et al. 2010 ). Also, epigenetic mechanisms may be an important component of an individual’s response to the environment ( Verhoeven et al. 2010 ). While these ideas are intriguing, few studies have made a clear connection between genome‐wide DNA methylation patterns and phenotypic plasticity (e.g. Bossdorf et al. 2010 ). In this issue of Molecular Ecology, Herrera et al. (2012) present a study that demonstrates epigenetic changes in genome‐wide DNA methylation are causally active in a species’ ability to exploit resources from a broad range of environments and are particularly important in harsh environments.     

Documenting DNA in the dust

I bought a robotic vacuum cleaner this summer and set it to work. Although my initial expectations were not high, my robot (christened Buddy) finished its cleaning cycle, and then insistently demanded that I empty its dust collection box. As I took the box out, my jaw dropped. I live in a modern house, we don't have pets, and I like to think that I keep it reasonably dust free. But, there was much dust in that box. And when I ran it again 2 days later, the same thing happened. And indeed, every 2 days, Buddy dutifully goes to work, and sucks up a similarly impressive quantity. It's remarkable, and naturally begs the question of where it all comes from? Some is externally derived, entering the house with us or through open windows. Some is clearly fibres shed from clothes, furniture etc. Then there's the skin cells and hair we shed. But at least part is derived from the host of smaller organisms that live in and around our homes, many of which are arthropods (Butte & Heinzow 2002 ). I suspect almost all readers are aware that some smaller animals live in our houses – even those who live in the modern urban houses will have occasionally encountered the odd drosophila, silverfish or spider. But I suspect that prior to reading Madden et al.'s article in this issue of Molecular Ecology (Madden et al. 2017 ), few of you will have appreciated the true diversity, which, it turns out, is huge.     

Loss of intestinal nuclei and intestinal integrity in aging C. elegans

The roundworm C. elegans is widely used as an aging model, with hundreds of genes identified that modulate aging (Kaeberlein et al., 2002. Mech. Ageing Dev. 123 , 1115–1119). The development and bodyplan of the 959 cells comprising the adult have been well described and established for more than 25 years ( Sulston & Horvitz, 1977 . Dev. Biol. 56 , 110–156; Sulston et al., 1983. Dev. Biol. 100 , 64–119.). However, morphological changes with age in this optically transparent animal are less well understood, with only a handful of studies investigating the pathobiology of aging. Age‐related changes in muscle ( Herndon et al., 2002 . Nature 419 , 808–814), neurons ( Herndon et al., 2002 ), intestine and yolk granules ( Garigan et al., 2002 . Genetics 161 , 1101–1112; Herndon et al., 2002 ), nuclear architecture ( Haithcock et al., 2005 . Proc. Natl Acad. Sci. USA 102 , 16690–16695), tail nuclei ( Golden et al., 2007 . Aging Cell 6 , 179–188), and the germline ( Golden et al., 2007 ) have been observed via a variety of traditional relatively low‐throughput methods. We report here a number of novel approaches to study the pathobiology of aging C. elegans. We combined histological staining of serial‐sectioned tissues, transmission electron microscopy, and confocal microscopy with 3D volumetric reconstructions and characterized age‐related morphological changes in multiple wild‐type individuals at different ages. This enabled us to identify several novel pathologies with age in the C. elegans intestine, including the loss of critical nuclei, the degradation of intestinal microvilli, changes in the size, shape, and cytoplasmic contents of the intestine, and altered morphologies caused by ingested bacteria. The three‐dimensional models we have created of tissues and cellular components from multiple individuals of different ages represent a unique resource to demonstrate global heterogeneity of a multicellular organism.