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 genetic dimension of pest pressure in the tropical rainforest

Wet tropical forests are among the most diverse ecosystems on Earth and can host several hundreds of tree species per hectare. To maintain such diversity, the community must contain large numbers of relatively rare species rather than be dominated by a few very common trees, as is often the case in temperate forests. Explaining the mechanisms preventing dominance by common species has been a major task of tropical forest ecology. One of the most promising mechanisms is negative density dependence (NDD) of tree abundance driven by pests, including fungal diseases (‘pest pressure’). NDD entails that the chance of survival of a sapling increases with the distance from a mature tree of the same species, thus preventing species from becoming locally dominant. Curiously, the strength of NDD is negatively correlated with abundance, meaning that tree species that are more common generally show weaker NDD (Comita et al. 2010 ). Interactions between plants and soil pathogens have been shown to play an important role in NDD (Klironomos 2002 ), and rare species are apparently more strongly affected (Mangan et al. 2010 ). However, the genetic mechanisms underlying this phenomenon have remained obscure. In this issue of Molecular Ecology, Marden et al. ( 2017 ) suggest that reduced diversity of the genes involved in pathogen recognition (Resistance genes or R genes) could explain why NDD is stronger in locally rare species.     

The shape of things to come in the study of the origin of species?

Perhaps Darwin would agree that speciation is no longer the mystery of mysteries that it used to be. It is now generally accepted that evolution by natural selection can contribute to ecological adaptation, resulting in the evolution of reproductive barriers and, hence, to the evolution of new species (Schluter & Conte 2009 ; Meyer 2011 ; Nosil 2012 ). From genes that encode silencing proteins that cause infertility in hybrid mice (Mihola et al. 2009 ), to segregation distorters linked to speciation in fruit flies (Phadnis & Orr 2009 ), or pollinator‐mediated selection on flower colour alleles driving reinforcement in Texan wildflowers (Hopkins & Rausher 2012 ), characterization of the genes that drive speciation is providing clues to the origin of species (Nosil & Schluter 2011 ). It is becoming apparent that, while recent work continues to overturn historical ideas about sympatric speciation (e.g. Barluenga et al. 2006 ), ecological circumstances strongly influence patterns of genomic divergence, and ultimately the establishment of reproductive isolation when gene flow is present (Elmer & Meyer 2011 ). Less clear, however, are the genetic mechanisms that cause speciation, particularly when ongoing gene flow is occurring. Now, in this issue, Franchini et al. ( 2014 ) employ a classic genetic mapping approach augmented with new genomic tools to elucidate the genomic architecture of ecologically divergent body shapes in a pair of sympatric crater lake cichlid fishes. From over 450 segregating SNPs in an F2 cross, 72 SNPs were linked to 11 QTL associated with external morphology measured by means of traditional and geometric morphometrics. Annotation of two highly supported QTL further pointed to genes that might contribute to ecological divergence in body shape in Midas cichlids, overall supporting the hypothesis that genomic regions of large phenotypic effect may be contributing to early‐stage divergence in Midas cichlids.     

Mock communities highlight the diversity of host‐associated eukaryotes

Host‐associated microbes are ubiquitous. Every multicellular eukaryote, and even many unicellular eukaryotes (protists), hosts a diverse community of microbes. High‐throughput sequencing (HTS) tools have illuminated the vast diversity of host‐associated microbes and shown that they have widespread influence on host biology, ecology and evolution (McFall‐Ngai et al. 2013 ). Bacteria receive most of the attention, but protists are also important components of microbial communities associated with humans (Parfrey et al. 2011 ) and other hosts. As HTS tools are increasingly used to study eukaryotes, the presence of numerous and diverse host‐associated eukaryotes is emerging as a common theme across ecosystems. Indeed, HTS studies demonstrate that host‐associated lineages account for between 2 and 12% of overall eukaryotic sequences detected in soil, marine and freshwater data sets, with much higher relative abundances observed in some samples (Ramirez et al. 2014 ; Simon et al. 2015 ; de Vargas et al. 2015 ). Previous studies in soil detected large numbers of predominantly parasitic lineages such as Apicomplexa, but did not delve into their origin [e.g. (Ramirez et al. 2014 )]. In this issue of Molecular Ecology, Geisen et al. ( 2015 ) use mock communities to show that many of the eukaryotic organisms detected by environmental sequencing in soils are potentially associated with animal hosts rather than free‐living. By isolating the host‐associated fraction of soil microbial communities, Geisen and colleagues help explain the surprisingly high diversity of parasitic eukaryotic lineages often detected in soil/terrestrial studies using high‐throughput sequencing (HTS) and reinforce the ubiquity of these host‐associated microbes. It is clear that we can no longer assume that organisms detected in bulk environmental sequencing are free‐living, but instead need to design studies that specifically enumerate the diversity and function of host‐associated eukaryotes. Doing so will allow the field to determine the role host‐associated eukaryotes play in soils and other environments and to evaluate hypotheses on assembly of host‐associated communities, disease ecology and more.     

Tree diversity in relation to maximum tree height: evidence for the harshness hypothesis of species diversity gradients

Marks et al. (Ecology Letters, 19, 2016, 743) showed tree species richness correlates with maximum tree height, and interpret this as evidence that the environmental stressors that limit tree height also act as ecological filters on species richness. Here, we strengthen these arguments by further addressing the roles of environmental covariates and beta diversity.     

Using RAD‐seq to recognize sex‐specific markers and sex chromosome systems

Next‐generation sequencing methods have initiated a revolution in molecular ecology and evolution (Tautz et al. 2010 ). Among the most impressive of these sequencing innovations is restriction site‐associated DNA sequencing or RAD‐seq (Baird et al. 2008 ; Andrews et al. 2016 ). RAD‐seq uses the Illumina sequencing platform to sequence fragments of DNA cut by a specific restriction enzyme and can generate tens of thousands of molecular genetic markers for analysis. One of the many uses of RAD‐seq data has been to identify sex‐specific genetic markers, markers found in one sex but not the other (Baxter et al. 2011 ; Gamble & Zarkower 2014 ). Sex‐specific markers are a powerful tool for biologists. At their most basic, they can be used to identify the sex of an individual via PCR. This is useful in cases where a species lacks obvious sexual dimorphism at some or all life history stages. For example, such tests have been important for studying sex differences in life history (Sheldon 1998 ; Mossman & Waser 1999 ), the management and breeding of endangered species (Taberlet et al. 1993 ; Griffiths & Tiwari 1995 ; Robertson et al. 2006 ) and sexing embryonic material (Hacker et al. 1995 ; Smith et al. 1999 ). Furthermore, sex‐specific markers allow recognition of the sex chromosome system in cases where standard cytogenetic methods fail (Charlesworth & Mank 2010 ; Gamble & Zarkower 2014 ). Thus, species with male‐specific markers have male heterogamety (XY) while species with female‐specific markers have female heterogamety (ZW). In this issue, Fowler & Buonaccorsi ( 2016 ) illustrate the ease by which RAD‐seq data can generate sex‐specific genetic markers in rockfish (Sebastes). Moreover, by examining RAD‐seq data from two closely related rockfish species, Sebastes chrysomelas and Sebastes carnatus (Fig.  1 ), Fowler & Buonaccorsi ( 2016 ) uncover shared sex‐specific markers and a conserved sex chromosome system.     

Homomorphic plant sex chromosomes are coming of age

Sex chromosomes are a very peculiar part of the genome that have evolved independently in many groups of animals and plants (Bull 1983 ). Major research efforts have so far been focused on large heteromorphic sex chromosomes in a few animal and plant species (Chibalina & Filatov 2011 ; Zhou & Bachtrog 2012 ; Bellott et al. 2014 ; Hough et al. 2014 ; Zhou et al. 2014 ), while homomorphic (cytologically indistinguishable) sex chromosomes have largely been neglected. However, this situation is starting to change. In this issue, Geraldes et al. ( 2015 ) describe a small (~100 kb long) sex‐determining region on the homomorphic sex chromosomes of poplars (Populus trichocarpa and related species, Fig.  1 ). All species in Populus and its sister genus Salix are dioecious, suggesting that dioecy and the sex chromosomes, if any, should be relatively old. Contrary to this expectation, Geraldes et al. ( 2015 ) demonstrate that the sex‐determining region in poplars is of very recent origin and probably evolved within the genus Populus only a few million years ago.     

Host plant richness explains diversity of ectomycorrhizal fungi: Response to the comment of Tedersoo et al. (2014)

Exploring the relationships between the biodiversity of groups of interacting organisms yields insight into ecosystem stability and function (Hooper et al. 2000 ; Wardle 2006 ). We demonstrated positive relationships between host plant richness and ectomycorrhizal (EM) fungal diversity both in a field study in subtropical China (Gutianshan) and in a meta‐analysis of temperate and tropical studies (Gao et al. 2013 ). However, based on re‐evaluation of our data sets, Tedersoo et al. ( 2014 ) argue that the observed positive correlation between EM fungal richness and EM plant richness at Gutianshan and also in our metastudies was based mainly from (i) a sampling design with inconsistent species pool and (ii) poor data compilation for the meta‐analysis. Accordingly, we checked our data sets and repeated the analysis performed by Tedersoo et al. ( 2014 ). In contrast to Tedersoo et al. ( 2014 ), our re‐analysis still confirms a positive effect of plant richness on EM fungal diversity in Gutianshan, temperate and tropical ecosystems, respectively.     

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.     

Getting specific: making taxonomic and ecological sense of large sequencing data sets

Eukaryotic microbes comprise a diverse collection of phototrophic and heterotrophic creatures known to play fundamental roles in ecological processes. Some can be identified by light microscopy, generally the largest and with conspicuous shapes, while the smallest can be counted by epifluorescence microscopy or flow cytometry but remain largely unidentified. Microbial diversity studies greatly advanced with the analysis of phylogenetic markers sequenced from natural assemblages. Molecular surveys began in 1990 targeting marine bacterioplankton (Giovannoni et al. 1990 ) and first approached microbial eukaryotes in three studies published in 2001 (Díez et al. 2001 ; López‐García et al. 2001 ; Moon‐van der Staay et al. 2001 ). These seminal studies, based on cloning and Sanger sequencing the complete 18S rDNA, were critical for obtaining broad pictures of microbial diversity in contrasted habitats and for describing novel lineages by robust phylogenies, but were limited by the number of sequences obtained. So, inventories of species richness in a given sample and community comparisons through environmental gradients were very incomplete. These limitations have been overcome with the advent of high‐throughput sequencing (HTS) methods, initially 454‐pyrosequencing, today Illumina and soon others to come. In this issue of Molecular Ecology, Egge et al. ( 2015 ) show a nice example of the use of HTS to study the biodiversity and seasonal succession of a particularly important group of marine microbial eukaryotes, the haptophytes. Temporal changes were analysed first at the community level, then at the clade level, and finally at the lowest rank comparable to species. Interesting and useful ecological insights were obtained at each taxonomic scale. Haptophyte diversity differed along seasons in a systematic manner, with some species showing seasonal preferences and others being always present. Many of these species had no correspondence with known species, pointing out the high level of novelty in microbial assemblages, only accessible by molecular tools. Moreover, the number of species detected was limited, agreeing with a putative scenario of constrained evolutionary diversification in free‐living small eukaryotes. This study illustrates the potential of HTS to address ecological relevant questions in an accessible way by processing large data sets that, nonetheless, need to be treated with a fair understanding of their limitations.     

Opportunities and challenges of next‐generation sequencing applications in ecological epigenetics

Evolutionary theory posits that adaptation can result when populations harbour heritable phenotypic variation for traits that increase tolerance to local conditions. However, the actual mechanisms that underlie heritable phenotypic variation are not completely understood (Keller 2014 ). Recently, the potential role of epigenetic mechanisms in the process of adaptive evolution has been the subject of much debate (Pigliucci & Finkelman 2014 ). Studies of variation in DNA methylation in particular have shown that natural populations harbour high amounts of epigenetic variation, which can be inherited across generations and can cause heritable trait variation independently of genetic variation (Kilvitis et al. 2014 ). While we have made some progress addressing the importance of epigenetics in ecology and evolution using methylation‐sensitive AFLP (MS‐AFLP), this approach provides relatively few anonymous and dominant markers per individual. MS‐AFLP are difficult to link to functional genomic elements or phenotype and are difficult to compare directly to genetic variation, which has limited the insights drawn from studies of epigenetic variation in natural nonmodel populations (Schrey et al. 2013 ). In this issue, Platt et al. provide an example of a promising approach to address this problem by applying a reduced representation bisulphite sequencing (RRBS) approach based on next‐generation sequencing methods in an ecological context.     

The genomics of adaptation,divergence and speciation: a congealing theory

In this issue, Flaxman et al. ( 2014 ) report the results of sophisticated whole‐genome simulations of speciation with gene flow, enhancing our understanding of the process by building on previous single‐locus, multilocus and analytical works. Their findings provide us with new insights about how genomes can diverge and the importance of statistical and chromosomal linkage in facilitating reproductive isolation. The authors characterize the conditions under which, even with high gene flow and weak divergent selection, reproductive isolation between populations can occur due to the emergent stochastic process of genomewide congealing, where numerous statistically or physically linked loci of small effect allow selection to limit effective migration rates. The initial congealing event can occur within a broad range conditions, and once initiated, the self‐reinforcing process leads to rapid divergence and ultimately two reproductively isolated populations. Flaxman et al.'s ( 2014 ) work is a valuable contribution to our understanding of speciation with gene flow and in making a more predictive field of evolutionary genomics and speciation.     

Why some parasites are widespread and abundant while others are local and rare?

Abundances and distributions of species are usually associated. This implies that as a species declines in abundance so does the number of sites it occupies. Conversely, when there is an increase in a species' range size, it is usually followed by an increase in population size (Gaston et al. 2000 ). This ecological phenomenon, also known as the abundance–occupancy relationship (AOR), is well documented in several species of animals and plants (Gaston et al. 2000 ) but has been little investigated in parasites. In this issue of Molecular Ecology, Drovetski et al. ( 2014 ) investigated the AOR in avian haemosporidians (vector‐borne blood parasites) using data from four well‐sampled bird communities. In support of the AOR, the research group found that the abundance of parasite cytochrome b lineages (a commonly used proxy for species identification within this group of parasites) was positively linked with the abundance of susceptible avian host species and that the most abundant haemospordian lineages were those with larger ranges. Drovetski et al. ( 2014 ) also found evidence for both hypotheses proposed to explain the AOR in parasites: the trade‐off hypothesis (TOH) and the niche‐breadth hypothesis (NBH). Interestingly, the main predictor of the AOR was the number of susceptible hosts (i.e. number of infected birds) and not the number of host species the parasites were able to exploit.     

Demystifying the RAD fad

We are writing in response to the population and phylogenomics meeting review by Andrews & Luikart ( 2014 ) entitled ‘Recent novel approaches for population genomics data analysis’. Restriction‐site‐associated DNA (RAD) sequencing has become a powerful and useful approach in molecular ecology, with several different published methods now available to molecular ecologists, none of which can be considered the best option in all situations. A&L report that the original RAD protocol of Miller et al. ( 2007 ) and Baird et al. ( 2008 ) is superior to all other RAD variants because putative PCR duplicates can be identified (see Baxter et al. 2011 ), thereby reducing the impact of PCR artefacts on allele frequency estimates (Andrews & Luikart 2014 ). In response, we (i) challenge the assertion that the original RAD protocol minimizes the impact of PCR artefacts relative to that of other RAD protocols, (ii) present additional biases in RADseq that are at least as important as PCR artefacts in selecting a RAD protocol and (iii) highlight the strengths and weaknesses of four different approaches to RADseq which are a representative sample of all RAD variants: the original RAD protocol (mbRAD, Miller et al. 2007 ; Baird et al. 2008 ), double digest RAD (ddRAD, Peterson et al. 2012 ), ezRAD (Toonen et al. 2013 ) and 2bRAD (Wang et al. 2012 ). With an understanding of the strengths and weaknesses of different RAD protocols, researchers can make a more informed decision when selecting a RAD protocol.     

THE BIOLOGY OF SPECIATION

Since Darwin published the “Origin,” great progress has been made in our understanding of speciation mechanisms. The early investigations by Mayr and Dobzhansky linked Darwin's view of speciation by adaptive divergence to the evolution of reproductive isolation, and thus provided a framework for studying the origin of species. However, major controversies and questions remain, including: When is speciation nonecological? Under what conditions does geographic isolation constitute a reproductive isolating barrier? and How do we estimate the “importance” of different isolating barriers? Here, we address these questions, providing historical background and offering some new perspectives. A topic of great recent interest is the role of ecology in speciation. “Ecological speciation” is defined as the case in which divergent selection leads to reproductive isolation, with speciation under uniform selection, polyploid speciation, and speciation by genetic drift defined as “nonecological.” We review these proposed cases of nonecological speciation and conclude that speciation by uniform selection and polyploidy normally involve ecological processes. Furthermore, because selection can impart reproductive isolation both directly through traits under selection and indirectly through pleiotropy and linkage, it is much more effective in producing isolation than genetic drift. We thus argue that natural selection is a ubiquitous part of speciation, and given the many ways in which stochastic and deterministic factors may interact during divergence, we question whether the ecological speciation concept is useful. We also suggest that geographic isolation caused by adaptation to different habitats plays a major, and largely neglected, role in speciation. We thus provide a framework for incorporating geographic isolation into the biological species concept (BSC) by separating ecological from historical processes that govern species distributions, allowing for an estimate of geographic isolation based upon genetic differences between taxa. Finally, we suggest that the individual and relative contributions of all potential barriers be estimated for species pairs that have recently achieved species status under the criteria of the BSC. Only in this way will it be possible to distinguish those barriers that have actually contributed to speciation from those that have accumulated after speciation is complete. We conclude that ecological adaptation is the major driver of reproductive isolation, and that the term “biology of speciation,” as proposed by Mayr, remains an accurate and useful characterization of the diversity of speciation mechanisms.     

Marine island biogeography. Response to comment on ‘Island biogeography: patterns of marine shallow‐water organisms’

In this response we have incorporated data on gastropod and seaweed biodiversity referred to by Ávila et al. (2016, Journal of Biogeography, doi: 10.1111/jbi.12816 ) to allow an updated analysis on marine shallow‐water biogeography patterns. When compared to the biogeography patterns reported in Hachich et al. (2015, Journal of Biogeography, 42 , 1871–1882), we find (1) no differences in the patterns originally reported for reef fish or seaweeds, (2) minor differences in gastropod species–area and species–age patterns and (3) a significant difference for the gastropod species‐isolation pattern. In our original work, we reported that there was limited evidence that gastropod species richness was influenced by island isolation; however, our new analysis reveals a power‐model relationship between these variables. Thus, we are now able to conclude that gastropod species diversity, whose dispersal capacity is intermediate between seaweeds (lowest) and reef fish (highest), is also influenced by island isolation.     

A robust tool highlights the influence of bird migration on influenza A virus evolution

One of the fundamental unknowns in the field of influenza biology is a panoramic understanding of the role wild birds play in the global maintenance and spread of influenza A viruses. Wild aquatic birds are considered a reservoir host for all lowly pathogenic avian influenza A viruses (AIV) and thus serve as a potential source of zoonotic AIV, such as Australasian‐origin H5N1 responsible for morbidity and mortality in both poultry and humans, as well as genes that may contribute to the emergence of pandemic viruses. Years of broad, in‐depth wild bird AIV surveillance have helped to decipher key observations and ideas regarding AIV evolution and viral ecology including the trending of viral lineages, patterns of gene flow within and between migratory flyways and the role of geographic boundaries in shaping viral evolution (Bahl et al. 2009 ; Lam et al. 2012 ). While these generally ‘virus‐centric’ studies have ultimately advanced our broader understanding of AIV dynamics, recent studies have been more host‐focused, directed at determining the potential impact of host behaviour on AIV, specifically, the influence of bird migration upon AIV maintenance and transmission. A large number of surveillance studies have taken place in Alaska, United States—a region where several global flyways overlap—with the aim of detecting the introduction of novel, Australasian‐origin highly pathogenic H5N1 AIV into North America. By targeting bird species with known migration habits, long‐distance migrators were determined to be involved in the intercontinental movement of individual AIV gene segments, but not entire viruses, between the Australasian and North American flyways (Koehler et al. 2008 ; Pearce et al. 2010 ). Yet, bird movement is not solely limited to long‐distance migration, and the relationship of resident or nonmigratory and intermediate‐distance migrant populations with AIV ecology has only recently been explored by Hill et al. ( 2012 ) in this issue of Molecular Ecology. Applying a uniquely refined, multidimensional approach, Hill et al. validate the innovative use of stable isotope assays for qualifying migration status of wild mallards within the Pacific flyway. The authors reveal that AIV prevalence and diversity did not differ in wintering mallard ducks with different migration strategies, and while migrant mallards do indeed introduce AIV, these viruses do not circulate as the predominant viruses in resident birds. On the other hand, resident mallards from more temperate regions act as reservoirs, possibly contributing to the unseasonal circulation and extended transmission period of AIV. This study highlights the impact of animal behaviour on shaping viral evolution, and the unique observations made will help inform prospective AIV surveillance efforts in wild birds.     

Tracking the elusive history of diversification in plant–herbivorous insect–parasitoid food webs: insights from figs and fig wasps

The food webs consisting of plants, herbivorous insects and their insect parasitoids are a major component of terrestrial biodiversity. They play a central role in the functioning of all terrestrial ecosystems, and the number of species involved is mind‐blowing (Nyman et al. 2015 ). Nevertheless, our understanding of the evolutionary and ecological determinants of their diversity is still in its infancy. In this issue of Molecular Ecology, Sutton et al. ( 2016 ) open a window into the comparative analysis of spatial genetic structuring in a set of comparable multitrophic models, involving highly species‐specific interactions: figs and fig wasps. This is the first study to compare genetic structure using population genetics tools in a fig‐pollinating wasp (Pleistodontes imperialis sp1) and its main parasitoid (Sycoscapter sp.A). The fig‐pollinating wasp has a discontinuous spatial distribution that correlates with genetic differentiation, while the parasitoid bridges the discontinuity by parasitizing other pollinator species on the same host fig tree and presents basically no spatial genetic structure. The full implications of these results for our general understanding of plant–herbivorous insect–insect parasitoids diversification become apparent when envisioned within the framework of recent advances in fig and fig wasp biology.     

Tending a complex microbiota requires major immune complexity

Animals maintain complex microbial communities within their guts that fill important roles in the health and development of the host. To what degree a host's genetic background influences the establishment and maintenance of its gut microbial communities is still an open question. We know from studies in mice and humans that external factors, such as diet and environmental sources of microbes, and host immune factors play an important role in shaping the microbial communities (Costello et al. 2012 ). In this issue of Molecular Ecology, Bolnick et al. ( 2014a ) sample the gut microbial community from 150 genetically diverse stickleback isolated from a single lake to provide evidence that another part of the adaptive immune response, the major histocompatibility complex class II (MHCII) receptors of antigen‐presenting cells, may play a role in shaping the gut microbiota of the threespine stickleback, Gasterosteus aculeatus (Bolnick et al. 2014a ). Bolnick et al. ( 2014a ) provide insight into natural, interindividual variation in the diversity of both stickleback MHCII alleles and their gut microbial communities and correlate changes in the diversity of MHCII receptor alleles with changes in the microbiota.