Sympatric speciation without borders?

The biogeography of speciation remains a controversial issue and the process of allopatric speciation reigns. Sympatric speciation differs from allopatric speciation in terms of geographic setting and the role of selection in bringing about reproductive isolating mechanisms, making it a particularly fascinating and controversial subject for evolutionary biologists. Mayr (1947) explained the difference eloquently: for allopatric speciation, populations spatially diverge and then become reproductively isolated; for sympatric speciation, populations first become reproductively isolated and then diverge. Because of this, sympatric speciation is difficult to show empirically and most evolutionary biologists agree that strict ecological, evolutionary, and geographic criteria must be met ( Coyne & Orr 2004 ). In this issue, Crow et al. (2010) challenge us to expand the definition of sympatric speciation by studying species of marine fishes that they propose have arisen by sympatric speciation in a setting that does not appear to conform to the usual geographical criteria.     

Digest: Process‐based phylogenetic models provide unique insights into the evolution of mutualistic networks*

Figs and their pollinating fig wasps are a classic example of long‐term obligate associations between different species. Satler et al. use a process‐based model adopted from molecular evolution to identify the major processes that affect cophylogenetic matching between figs and fig wasps. They find that host‐switching is one of the most important evolutionary processes contributing to current cophylogenetic patterns, illustrating the value of probabilistic approaches to studying the evolutionary history of mutualisms.     

Stasipatric speciation: resurrecting a system to bury a hypothesis?

The process of speciation remains a fundamental topic in evolutionary biology. Numerous models of speciation have been proposed and they are as diverse and colourful as the scientists who conceived them ( Coyne & Orr 2004 ). One of the more controversial theories has been the ‘stasipatric speciation’ model, proposed by the pioneering and influential cytogeneticist Michael White and his co‐workers ( White 1968 ; White et al. 1967 ). This is one of a number of speciation models whereby chromosomal rearrangements drive the speciation process. The inspiration for the theory of stasipatric speciation came from White’s karyotypic analyses of a group of Australian grasshoppers of the genus Vandiemenella ( White et al. 1967 ) ( Fig. 1 ). It has been exactly three decades since the last scientific publication on this group of grasshoppers, over which time the molecular revolution dramatically altered the landscape of evolutionary genetics. Kawakami and colleagues have successfully resurrected the Vandiemenella system ( Kawakami et al. 2009a, 2007 ) and in this issue they have applied modern molecular‐based techniques to reassess the validity of the stasipatric speciation model for this historically important group ( Kawakami et al. 2009b ).

Figure 1 Open in figure viewer PowerPoint The grasshopper (Vandiemenella viatica) that inspired Michael White to develop the stasipatric speciation model (photograph by Remko Leijs).     

When structure leads to sex: Untangling signals in population genetic data sets

A robust signal of population structure often provides the first glimpse into the evolutionary history of a species and its populations. In this issue of Molecular Ecology, new work from Louis Bernatchez's group (Benestan et al., 2017 ) starts with an investigation of apparent structure in two marine species and concludes with an identification of sex‐linked genes, and in the process provides a model for robust analysis. Structure is the genetic signal left by natural selection as well as by neutral processes like migration and gene flow. Neutral areas of the genome can reveal the geographical relationships and related gene flow between populations over time and space, while selection can resist the natural genomic turnover created by recombination and generate adaptive structure between populations that can be detected. However, artefacts in a data set can easily hide the true signal of structure; mutation, whether it is a true appearance of a recent, minor allele, or more commonly, an error in SNP calling or molecular library construction, can easily conceal patterns of population structure (e.g., geographical structure in mackerel, Rodriguez‐Ezpeleta et al. ( 2016 )). A demographic structure that results from the most “forceful” evolutionary processes can overwhelm another signal generated by other, unrelated phenotypes. For example, the structure among diverged freshwater and marine threespine stickleback populations results from such strong selection and linkage disequilibrium across the genome that it impairs the ability to disentangle the genetic basis of particular evolved morphological traits (e.g., opercle development, Alligood ( 2017 )). Finally, there might be conflicting inferences for what underlies structure patterns. Structure may be created by differential patterns of meiotic recombination, and genetic maps are a reliable means for identifying genomic regions that resist recombination. But, without additional information (Anderson et al., 2012 ), it can be difficult to distinguish the recombination‐suppressing effect of a segregating genomic inversion (Small et al., 2016 ) from that of sex‐linked selection.     

Assessing community and ecosystem sensitivity to climate change – toward a more comparative approach

Plant communities can vary widely in their sensitivity to changing precipitation regimes, as reported by Byrne et al., Mulhouse et al. and Sternberg et al. in this issue of Journal of Vegetation Science. But to understand why communities differ in their sensitivity, we argue that clearly defined metrics of sensitivity and coordinated research approaches are needed to elucidate mechanisms.     

Microbiome maturation during a unique developmental window

Shortly after birth, mammals are colonized by a multitude of microbes derived from the mother and the environment. Studies in model organisms have demonstrated that the structure and composition of the gut microbiome of offspring steadily mature with increasing diversity during nursing and weaning (Sommer & Bäckhed, 2013). This period of microbiome assembly is critical for young mammals because the gut microbes they acquire will help train their immune system (Lathrop et al., 2011) with potential long‐lasting effects on their health (Cox et al., 2014). In an article in this issue of Molecular Ecology, Stoffel et al. (2020) investigated the gut microbiota of northern elephant seals (Mirounga angustirostris) during a key developmental window. A month after giving birth, elephant seal mothers stop nursing their pups and return to the sea. As a consequence, their pups go from a diet of milk rich in fat to abruptly enter a post weaning fasting period which lasts for about two months while they remain with the colony. This particular life‐history trait therefore offered the authors a unique and exciting opportunity to evaluate intrinsic factors contributing to gut microbiota development in a wild marine mammal.     

Biases in assessing the evolutionary history of the angiosperm flora of China

In their recent paper published in Nature (2018, 554, 234‐238), Lu et al. use phylogenetic approaches to determine the proportion of the Chinese angiosperm genera that originated during the Miocene or later, and contrast divergence times and phylogenetic dispersion between eastern and western China. One of their key conclusions is that 66% of the angiosperm genera in China originated in the Miocene or later. However, an analysis of 300 angiosperm genera shows that 139 (76.8%) of the 181 genera considered as originating in the Miocene or later by Lu et al. have fossil records before the Miocene. Thus, the evolutionary history of Chinese angiosperm flora has been substantially underestimated in Lu et al. In addition, the results of Lu et al. have been biased by using an incomplete phylogeny.     

Implications of uniformly distributed,empirically informed priors for phylogeographical model selection: A reply to Hickerson et al.

Establishing that a set of population‐splitting events occurred at the same time can be a potentially persuasive argument that a common process affected the populations. Recently, Oaks et al. ( 2013 ) assessed the ability of an approximate‐Bayesian model‐choice method (msBayes ) to estimate such a pattern of simultaneous divergence across taxa, to which Hickerson et al. ( 2014 ) responded. Both papers agree that the primary inference enabled by the method is very sensitive to prior assumptions and often erroneously supports shared divergences across taxa when prior uncertainty about divergence times is represented by a uniform distribution. However, the papers differ about the best explanation and solution for this problem. Oaks et al. ( 2013 ) suggested the method's behavior was caused by the strong weight of uniformly distributed priors on divergence times leading to smaller marginal likelihoods (and thus smaller posterior probabilities) of models with more divergence‐time parameters (Hypothesis 1); they proposed alternative prior probability distributions to avoid such strongly weighted posteriors. Hickerson et al. ( 2014 ) suggested numerical‐approximation error causes msBayes analyses to be biased toward models of clustered divergences because the method's rejection algorithm is unable to adequately sample the parameter space of richer models within reasonable computational limits when using broad uniform priors on divergence times (Hypothesis 2). As a potential solution, they proposed a model‐averaging approach that uses narrow, empirically informed uniform priors. Here, we use analyses of simulated and empirical data to demonstrate that the approach of Hickerson et al. ( 2014 ) does not mitigate the method's tendency to erroneously support models of highly clustered divergences, and is dangerous in the sense that the empirically derived uniform priors often exclude from consideration the true values of the divergence‐time parameters. Our results also show that the tendency of msBayes analyses to support models of shared divergences is primarily due to Hypothesis 1, whereas Hypothesis 2 is an untenable explanation for the bias. Overall, this series of papers demonstrates that if our prior assumptions place too much weight in unlikely regions of parameter space such that the exact posterior supports the wrong model of evolutionary history, no amount of computation can rescue our inference. Fortunately, as predicted by fundamental principles of Bayesian model choice, more flexible distributions that accommodate prior uncertainty about parameters without placing excessive weight in vast regions of parameter space with low likelihood increase the method's robustness and power to detect temporal variation in divergences.     

Evolutionary ecology of opsin gene sequence,expression and repertoire

Linking molecular evolution to biological function is a long‐standing challenge in evolutionary biology. Some of the best examples of this involve opsins, the genes that encode the molecular basis of light reception. In this issue of Molecular Ecology, three studies examine opsin gene sequence, expression and repertoire to determine how natural selection has shaped the visual system. First, Escobar‐Camacho et al. ( 2017 ) use opsin repertoire and expression in three Amazonian cichlid species to show that a shift in sensitivity towards longer wavelengths is coincident with the long‐wavelength‐dominated Amazon basin. Second, Stieb et al. ( 2017 ) explore opsin sequence and expression in reef‐dwelling damselfish and find that UV‐ and long‐wavelength vision are both important, but likely for different ecological functions. Lastly, Suvorov et al. ( 2017 ) study an expansive opsin repertoire in the insect order Odonata and find evidence that copy number expansion is consistent with the permanent heterozygote model of gene duplication. Together these studies emphasize the utility of opsin genes for studying both the local adaptation of sensory systems and, more generally, gene family evolution.     

Antarctic macrolichen modifies microclimate and facilitates vascular plants in the maritime Antarctica – a reply to Casanova‐Katny et al. (2014)

In a current article in the Journal of Vegetation Science, Casanova‐Katny et al. addressed a comment about an article by Molina‐Montenegro et al., which demonstrated the climate modification induced by the macrolichen Usnea antarctica and its role as facilitator. They provided useful corrections concerning species identification and pointed out several issues that, in their view, weakened our study. They indicated that the role of U. antarctica as a facilitative species in the maritime Antarctica is merely philosophical and has no ecological relevance. In this commentary, we argue why these critiques are unsubstantial, and provide evidence that the macrolichen can modify the microclimate, ameliorating the harsh conditions prevailing in Antarctica, establishing positive interactions and eventually facilitating vascular species. Thus, the macrolichen U. antarctica would act as a ‘nurse species’, playing a key role in structuring the maritime Antarctic plant community.     

Mutually exclusive phylogenomic inferences at the root of the angiosperms: Amborella is supported as sister and Observed Variability is biased

Identifying the extant sister group to the remaining angiosperms has been a subject of long debate, for which the primary currently competing hypotheses are that Amborella alone is sister or that the clade (Amborella, Nymphaeales) is sister. Both Xi et al. (Syst. Biol., 2014, 63, 919) and Goremykin et al. (Syst. Biol., 2015, 64, 879) identified Amborella as sister in concatenation‐based phylogenetic analyses of their 310 nuclear genes and 78 plastid genes, respectively. But after application of Observed Variability‐based character subsampling, both papers reported the clade (Amborella, Nymphaeales) as sister. Hence alternative character‐sampling strategies may produce highly supported yet mutually exclusive phylogenetic inferences when applied to nuclear and plastid genomic data sets. Edwards et al. (Mol. Phylogenet. Evol., 2016, 94, 447) defended Observed Variability and the (Amborella, Nymphaeales) hypothesis. In this study I respond to Edwards et al.'s (Mol. Phylogenet. Evol., 2016, 94, 447) criticisms of Simmons and Gatesy (Mol. Phylogenet. Evol., 2015, 91, 98) and use Edwards et al.'s (Mol. Phylogenet. Evol., 2016, 94, 447) and Goremykin et al.'s (Syst. Biol., 2015, 64, 879) own data to demonstrate that the best‐supported phylogenetic hypothesis is that Amborella alone is sister and that the competing evidence in favour of the (Amborella, Nymphaeales) hypothesis is caused primarily by methodological artifacts (biased character deletion by Observed Variability, MP‐EST and STAR generally not being robust to the highly divergent and mis‐rooted gene trees that were used).     

Digest: Little evidence exists for a virulence‐transmission trade‐off*

Research predicting the impact and spread of infectious disease has been heavily influenced by the idea of an evolutionary trade‐off between a pathogen's virulence and its transmission rate. In a meta‐analysis of the key underlying relationships, Acevedo et al. (2019) highlight the surprising lack of empirical evidence for this influential hypothesis.     

Searching for the genetic footprint of ancient and recent hybridization

Determining the long‐term consequences of hybridization remains a central quest for evolutionary biologists. A particular challenge is to establish whether and to what extent widespread hybridization results in gene flow (introgression) between parental taxa. In this issue of Molecular Ecology, Jordan et al. ( 2018 ) search for evidence of gene flow between two closely related species of Geum (Rosaceae), which hybridize readily in contemporary populations and where hybrid swarms have been recorded for at least 200 years (Ruhsam, Hollingsworth, & Ennos, 2013 ). The authors find mixed evidence of ancient introgression when analysing allopatric populations. Intriguingly, when analysing populations of a region where the two species occur either mixed in the same population or in close proximity, and where hybrids are presently common, Jordan and colleagues find that the majority of randomly sampled individuals analysed (92/96) show no evidence of introgression (defined as individuals with admixture coefficients of <1%). The few individuals identified as hybrids are shown to likely be F1 or early‐generation backcrosses, indicating that even in sympatric regions, hybridization does not penetrate beyond a few generations. Based on their findings, Geum seems to be an example of little to no introgression despite contemporary hybridization.     

Sexual conflict and the maintenance of genetic variation in natural populations

Understanding the factors that maintain genetic variation in natural populations is a foundational goal of evolutionary biology. To this end, population geneticists have developed a variety of models that can produce stable polymorphisms. In one of the earliest models, Owen ( 1953 ) demonstrated that differences in selection pressures acting on males and females could maintain multiple alleles of a gene at a stable equilibrium. If the selection pressures act in opposite directions in males and females, we refer to this as (inter‐) sexual conflict or sexual antagonism (Arnqvist & Rowe, 2005 ). Testing if sexual conflict maintains genetic variation in natural populations is a tremendous challenge—it requires both identifying loci that harbor sexually antagonistic alleles and determining whether those alleles are maintained as stable polymorphisms (Mank, 2017 ). Doing so genome‐wide is even harder because it is not tractable to identify sexually antagonistic alleles and test for stable polymorphisms at all loci. Dutoit et al. ( 2018 ) confront this challenge in a paper published in this issue of Molecular Ecology. Using gene expression and population genomic data from the collared flycatcher, Dutoit et al. ( 2018 ) identify associations and correlations between genomic signatures of balanced polymorphisms and sexual conflict.     

Two are better than one: combining landscape genomics and common gardens for detecting local adaptation in forest trees

Predicting likely species responses to an alteration of their local environment is key to decision‐making in resource management, ecosystem restoration and biodiversity conservation practice in the face of global human‐induced habitat disturbance. This is especially true for forest trees which are a dominant life form on Earth and play a central role in supporting diverse communities and structuring a wide range of ecosystems. In Europe, it is expected that most forest tree species will not be able to migrate North fast enough to follow the estimated temperature isocline shift given current predictions for rapid climate warming. In this context, a topical question for forest genetics research is to quantify the ability for tree species to adapt locally to strongly altered environmental conditions (Kremer et al. 2012 ). Identifying environmental factors driving local adaptation is, however, a major challenge for evolutionary biology and ecology in general but is particularly difficult in trees given their large individual and population size and long generation time. Empirical evaluation of local adaptation in trees has traditionally relied on fastidious long‐term common garden experiments (provenance trials) now supplemented by reference genome sequence analysis for a handful of economically valuable species. However, such resources have been lacking for most tree species despite their ecological importance in supporting whole ecosystems. In this issue of Molecular Ecology, De Kort et al. ( 2014 ) provide original and convincing empirical evidence of local adaptation to temperature in black alder, Alnus glutinosa L. Gaertn, a surprisingly understudied keystone species supporting riparian ecosystems. Here, De Kort et al. ( 2014 ) use an innovative empirical approach complementing state‐of‐the‐art landscape genomics analysis of A. glutinosa populations sampled in natura across a regional climate gradient with phenotypic trait assessment in a common garden experiment (Fig. 1 ). By combining the two methods, De Kort et al. ( 2014 ) were able to detect unequivocal association between temperature and phenotypic traits such as leaf size as well as with genetic loci putatively under divergent selection for temperature. The research by De Kort et al. ( 2014 ) provides valuable insight into adaptive response to temperature variation for an ecologically important species and demonstrates the usefulness of an integrated approach for empirical evaluation of local adaptation in nonmodel species (Sork et al. 2013 ).     

The importance of genomic novelty in social evolution

Insect societies dominate the natural world: They mould landscapes, sculpt habitats, pollinate plants, sow seeds and control pests. The secret to their success lies in the evolution of queen (reproductive) and worker (provisioner and carer) castes (Oster & Wilson 1978 ). A major problem in evolutionary biology is explaining the evolution of insect castes, particularly the workers (Darwin 1859 ). Next‐generation sequencing technologies now make it possible to understand how genomic material is born, lost and reorganized in the evolution of alternative phenotypes. Such analyses are revealing a general role for novel (e.g. taxonomically restricted) genes in phenotypic innovations across the animal kingdom (Chen et al. 2013). In this issue of molecular ecology, Feldmeyer et al. (2014) provide overwhelming evidence for the importance of novel genes in caste evolution in an ant. Feldmeyer et al.'s study is important and exciting because it cements the role of genomic novelty, as well as conservation, firmly into the molecular jigsaw of social evolution. Evolution is eclectic in its exploitation of both old and new genomic material to generate replicated phenotypic innovations across the tree of life.     

Cryptic diversity and patterns of host specificity in trematode flatworms

The widespread utilization of molecular markers has revealed that a broad spectrum of taxa contain sets of morphologically cryptic, but genetically distinct lineages ( Bickford et al. 2007 ). The identification of cryptic taxa is important as an accurate appreciation of diversity is crucial for a proper understanding of evolutionary and ecological processes. An example is the study of host specificity in parasitic taxa, where an apparent generalist may be found to contain a complex of several more specific species ( Smith et al. 2006 ). Host specificity is a key life history trait that varies greatly among parasites ( Poulin & Keeney 2007 ). While some can exploit a wide range of hosts, others are confined to just a single species. Access to additional hosts increases the resources available to a parasite. However, physiological or ecological constraints can restrict the extension of host range. Furthermore, there may be a trade‐off between relaxed specificity and performance: generalism can decrease a parasites ability to adapt to each individual host species, and increase exposure to competition from other parasites ( Poulin 1998 ). Despite the central role that host specificity plays in parasite life history, relatively little is known about how host range is determined in natural systems, and data from field studies are required to evaluate among competing ideas. In this issue, an exciting paper by Locke et al. (2010) makes a valuable contribution toward the understanding of host specificity in an important group of trematode flatworms. Using molecular methods, Locke et al. reveal an almost four‐fold increase in the appreciated diversity of their focal group. In combination with a large and elegant sampling design this allows them to accurately assess host specificity for each taxon, and thus draw key insights into the factors that control host range in a dominant parasite group.     

From transects to transcripts: Teasing apart the architecture of reproductive isolation

Understanding the processes underlying speciation has long been a challenge to evolutionary biologists. This spurs from difficulties teasing apart the various mechanisms that contribute to the evolution of barriers to reproduction. The study by Rafati et al. ( 2018 ) in this issue of Molecular Ecology combines spatially explicit whole‐genome resequencing with evaluation of differential gene expression across individuals with mixed ancestry to associate the genomic architecture of reproductive barriers with expression of reproductive incompatibilities. In a natural hybrid zone between rabbit subspecies, Oryctolagus cuniculus cuniculus and O. c. algirus (Figure  1 ), Rafati et al. ( 2018 ) use landscape‐level patterns of allele frequency variation to identify potential candidate regions of the genome associated with reproductive isolation. These candidate regions are used to test predictions associated with the genomic architecture of reproductive barriers, including the role of structural rearrangements, enrichment of functional categories associated with incompatibilities, and the contribution of protein‐coding versus regulatory changes. A lack of structural rearrangements and limited protein‐coding changes in candidate regions point towards the importance of regulatory variation as major contributors to genetic incompatibilities, while functional enrichments indicate overrepresentation of genes associated with male infertility. To quantify phenotypic expression of proposed incompatibilities, the authors assess gene expression of experimental crosses. Extensive misregulation of gene expression within the testes of backcross hybrids relative to F1 and parental individuals provides an important link between genotype and phenotype, validating hypotheses developed from assessment of genomic architectures. Together, this work shows how pairing natural hybrid zones with experimental crosses can be used to link observations in nature to mechanistic underpinnings that may be tested experimentally.     

Exploiting plants for glutathione (GSH) production: Uncoupling GSH synthesis from cellular controls results in unprecedented GSH accumulation

Glutathione (GSH) is a key factor for cellular redox homeostasis and tolerance against abiotic and biotic stress ( May et al., 1998 ; Noctor et al., 1998a ). Previous attempts to increase GSH content in plants have met with moderate success ( Rennenberg et al., 2007 ), largely because of tight and multilevel control of its biosynthesis ( Rausch et al., 2007 ). Here, we report the in planta expression of the bifunctional γ‐glutamylcysteine ligase—glutathione synthetase enzyme from Streptococcus thermophilus (StGCL‐GS), which is shown to be neither redox‐regulated nor sensitive to feedback inhibition by GSH. Transgenic tobacco plants expressing StGCL‐GS under control of a constitutive promoter reveal an extreme accumulation of GSH in their leaves (up to 12 μmol GSH/gFW, depending on the developmental stage), which is more than 20‐ to 30‐fold above the levels observed in wild‐type (wt) plants and which can be even further increased by additional sulphate fertilization. Surprisingly, this dramatically increased GSH production has no impact on plant growth while enhancing plant tolerance to abiotic stress. Furthermore, StGCL‐GS‐expressing plants are a novel, cost‐saving source for GSH production, being competitive with current yeast‐based systems ( Li et al., 2004 ).