Evolutionary potential in the wild: more than meets the eye

The genus Aquilegia consists of 60–70 perennial plant species widely distributed throughout the northern hemisphere. Its flowers have a delicate and ornamental appearance that makes them a favourite of gardeners. In this genus, adaptive radiations for both floral and vegetative traits have occurred. These adaptive radiations, and the key phylogenetic placement of Aquilegia between Arabidopsis and rice, make this genus a ‘model system’ for plant evolution ( Kramer 2009 ). In this issue, Castellanos et al. (2011) use a marker‐based method to infer heritability for floral and vegetative traits in two Aquilegia species. Layered on top of this are estimates of the strength of natural selection. This novel joint estimation of heritability and selection in the wild showed that vegetative traits, compared to floral traits, have the highest evolutionarily potential. Evolutionary potential is the most important quantity to measure in wild populations. It combines inheritance and strength of selection and predicts the potential for populations to adapt to changing environments. The combination of molecular techniques with species in natural environments makes this work a model for molecular ecological investigations.     

Making inferences about speciation using sophisticated statistical genetics methods: look before you leap

Understanding speciation is a fundamental aim of evolutionary biology and a very challenging one. Speciation can be viewed as the dynamics of genetic differentiation between populations resulting in substantial reproductive isolation (Gavrilets 2003). It was generally accepted that very small levels of migration prevent genetic differentiation among populations and, therefore, speciation. However, recent theoretical work showed that sympatric speciation is possible (Gavrilets 2003). Nevertheless, providing empirical evidence that gene flow occurred during speciation is challenging because several gene flow scenarios can explain observed patterns of genetic differentiation. Positive migration rate estimates alone do not prove ongoing gene flow during divergence. We also need to know whether migration took place before, during or after speciation. There is no statistical method specifically aimed at estimating gene flow timing, but several studies used the isolation with migration model (Hey & Nielsen 2004, 2007; Hey 2010b) to estimate this parameter and make inferences about speciation scenarios. It is tempting to use statistical methods to estimate important evolutionary parameters even if they do not appear explicitly in the inference model. Nevertheless, before doing so, we need to determine whether they can provide reliable results. In this issue of Molecular Ecology, Strasburg and Rieseberg (2011) present a simulation study that examines the degree to which gene flow timing estimates obtained from IMa2 (Hey 2010b) can be used to make inferences about speciation mode. Their results are sobering; gene flow timing estimates obtained in this way are not reliable and cannot be used to unequivocally establish if gene flow was ongoing during speciation.     

The genetic basis of evolution, adaptation and speciation

A primary question in biology concerns the genetic basis of the evolution of novel traits, often in response to environmental changes, and how this can subsequently cause species isolation. This topic was the focus of the symposium on the Genetics of Speciation and Evolution at the annual meeting of the Canadian Society for Ecology and Evolution, held in Banff in May 2011. The presentations revealed some of the rapid advances being made in understanding the genetic basis of adaptation and speciation, as well as the elegant interplay between an organism's genetic complement and the environment that organism experiences.     

Notes from a snail island: Littorinid evolution and adaptation

The most successful study systems are built on a foundation of decades of research on the basic biology, ecology and life history of the organisms in question. Combined with new technologies, this can provide a formidable means to address important issues in evolutionary biology and molecular ecology. Littorinid marine snails are a good example of this, with a rich literature on their taxonomy, speciation, thermal tolerance and behavioural adaptations. In August 2017, an international meeting on Littorinid evolution was held at the Tjärnö Marine Research Laboratory in Western Sweden. In this meeting review, I provide a summary of some of the exciting work on parallel evolution, sexual selection and adaptation to environmental stress presented there. I argue that newly available genomic resources present an opportunity for integrating the traditionally divergent fields of speciation and environmental adaptation in Littorinid research.     

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     

Proceedings of the SMBE Tri-National Young Investigators' Workshop 2005. Molecular genetics of natural populations

Significant progress in evolutionary genetics has been made by studying, on the one hand, patterns of DNA sequence polymorphism and, on the other, genetic architecture of complex adaptive traits. However, connections between nucleotide variants under selection and adaptively relevant phenotypes are missing. Such connections can be established using precise gene replacement. We review the recent successful introduction of this technique to the analysis of two evolutionarily interesting loci--Odysseus and desaturase2. Both genes have subtle phenotypes that nevertheless could be identified using gene replacement, demonstrating that effects of naturally occurring alleles can be measured in the laboratory. This is an important first step in connecting statistical signatures of selection with adaptation in nature. More candidate genes involved in adaptation, for example, through cloning of genes responsible for reproductive isolation, now need to be identified. Molecular genetic manipulation, DNA polymorphism analysis, and field studies then have to be integrated to provide fresh insights into the mechanisms of evolutionary change.     

Adaptation with gene flow across the landscape in a dune sunflower

Isolation by adaptation increases divergence at neutral loci when natural selection against immigrants reduces the rate of gene flow between different habitats. This can occur early in the process of adaptive divergence and is a key feature of ecological speciation. Despite the ability of isolation by distance (IBD) and other forms of landscape resistance to produce similar patterns of neutral divergence within species, few studies have used landscape genetics to control for these other forces. We have studied the divergence of Helianthus petiolaris ecotypes living in active sand dunes and adjacent non-dune habitat, using landscape genetics approaches, such as circuit theory and multiple regression of distance matrices, in addition to coalescent modelling. Divergence between habitats was significant, but not strong, and was shaped by IBD. We expected that increased resistance owing to patchy and unfavourable habitat in the dunes would contribute to divergence. Instead, we found that landscape resistance models with lower resistance in the dunes performed well as predictors of genetic distances among subpopulations. Nevertheless, habitat class remained a strong predictor of genetic distance when controlling for isolation by resistance and IBD. We also measured environmental variables at each site and confirmed that specific variables, especially soil nitrogen and vegetation cover, explained a greater proportion of variance in genetic distance than did landscape or the habitat classification alone. Asymmetry in effective population sizes and numbers of migrants per generation was detected using coalescent modelling with Bayesian inference, which is consistent with incipient ecological speciation being driven by the dune habitat.