As sea surface temperature increases, many coral species that used to harbor symbionts of the genus Cladocopium have become colonized with the thermally tolerant genus, Durusdinium. Here, we asked how symbionts of one genus react to the presence of another symbiont genus within the same coral host, and what effect this has on the host. We used previously published data from Acropora hyacinthus corals hosting Cladocopium and/or Durusdinium symbionts and looked at gene expression in all three symbiotic partners depending on the relative proportions of symbiont genera within the host. We find that both Cladocopium and Durusdinium change their expression most when their proportions are nearly equal (the state that we call “codominance”): both genera elevate expression of photosynthesis and ribosomal genes, suggesting increase in photosynthesis and growth (i.e. higher productivity). At the same time, the coral host also elevates production of ribosomes suggesting faster cellular growth, and, when heated, shows less pronounced stress response. These results can be explained in two ways. One explanation is that increased competition between symbionts heightens their productivity, which benefits the host, making it more resilient to stress. Alternatively, the symbionts’ elevated productivity might be the consequence of the host being particularly healthy. Under this explanation, rapid growth of the healthy host creates new space, lowering the symbionts’ competition and allowing for codominance. The latter explanation is supported by the fact that codominance is associated with lower symbiont densities. Irrespective of the causation, the presence of mixed symbiont communities could potentially be used as an instant indicator of coral well-being, which would be a useful tool for coral conservation and restoration.
A recent Molecular Ecology editorial made a proactive statement of support for the “Nagoya Protocol” and the principle of benefit-sharing (Marden et al. 2020) by requiring authors to provide a “Data Accessibility and Benefit‐Sharing Statement” in their articles. Here, we encourage another step that enables Indigenous communities to provide their own definitions and aspirations for access and benefit-sharing alongside the author’s “Statement”. We invite the Molecular Ecology research community to use Biocultural-, Traditional Knowledge-, and Cultural Institution Notices to help Indigenous communities gain visibility within our research structures. Notices are one of the tools offered by the Biocultural Labels Initiative (part of the Local Contexts system) designed specifically for researchers and institutions. The Notices are highly visible, machine-readable icons that signal the Indigenous provenance of genetic resources, and rights of Indigenous communities to define the future use of genetic resources and derived benefits. The Notices invite collaboration with Indigenous communities and create spaces within our research systems for them to define the provenance, protocols, and permissions associated with genetic resources using Labels. Authors contributing to Molecular Ecology can apply Notices to their articles by providing the persistent unique identifier and an optional use-statement associated with the Notice in their “Data Accessibility and Benefit‐Sharing Statement”. In this way, our research community has an opportunity to accelerate support for the principles of the Nagoya Protocol, to alleviate concerns regarding Indigenous Data Sovereignty and equitable outcomes, and to build better relationships with Indigenous collaborators to enhance research, biodiversity, and conservation outcomes.
Telomeres have been advocated to be important markers of biological age in evolutionary and ecological studies. Telomeres usually shorten with age, and shortening is frequently associated with environmental stressors and increased subsequent mortality. Telomere lengthening – an apparent increase in telomere length between repeated samples from the same individual – also occurs. However, the exact circumstances, and consequences, of telomere lengthening are poorly understood. Using longitudinal data from the Seychelles warbler (Acrocephalus sechellensis), we tested whether telomere lengthening – which occurs in adults of this species – is associated with specific stressors (reproductive effort, food availability, malarial infection and cooperative breeding) and predicts subsequent survival. In females, telomere shortening was observed under greater stress (i.e. low food availability, malaria infection), while telomere lengthening was observed in females experiencing lower stress (i.e. high food availability, assisted by helpers, without malaria). The telomere dynamics of males were not associated with the key stressors tested. These results indicate that, at least for females, telomere lengthening occurs in circumstances more conducive to self-maintenance. Importantly, both females and males with lengthened telomeres had improved subsequent survival relative to individuals that displayed unchanged, or shortened, telomeres – indicating that telomere lengthening is associated with individual fitness. These results demonstrate that telomere dynamics are bidirectionally responsive to the level of stress that an individual faces, but may poorly reflect the accumulation of stress over the lifetime. This study challenges how we think of telomeres as a marker of biological age.
Globalization and international trade have impacted organisms around the world leading to a considerable number of species establishing in new geographic areas. Many organisms have taken advantage of human-made environments, including buildings. One such species is the dry rot fungus Serpula lacrymans, which is the most aggressive wood-decay fungus in indoor environments in temperate regions. By using population genomic analyses of 36 full genome sequenced isolates, we revealed that isolates from Europe and Japan are highly divergent and that these populations split 3,000 - 19,000 generations ago, probably predating human influence. Approximately 250 generations ago, the European population went through a tight bottleneck, likely corresponding to the time it colonized the built environment. Moreover, evidence of admixture between European and Japanese populations was shown in an isolate from New Zealand. Genomic analyses revealed that low differentiation appeared in genes with functions related to of growth and intracellular transport, possibly important to its ability to effectively decay large substrates. These functions may have enabled both populations to independently establish in the human-made environment. Further, selective sweep analyses identified rapid changes in genes possibly related to decay of various substrates in Japan and in genes involved DNA replication and protein modification in Europe. These two fungal populations were preadapted to the built environment, but have more recently and independently adapted to their local environment.
Barriers to gene flow (BGF) play a pivotal role in the dynamics of population genetics promoting genetic differentiation, thus, are inexorably associated with the development and maintenance of phylogeographic structure. Phylogeographic structure resulting from BGF represents data that help the management of natural genetic resources, aiding in the recognition of areas of conservation interest. Several geographic and oceanographic processes found along the Brazilian coast have been proposed as BGF. However, no consensus exist identifying which of them represents the most important in shaping biodiversity. Therefore, this study provides a synthesis of the scientific literature on Brazilian marine phylogeography and used published data to build datasets that allowed us apply linear (lm) and generalized additive models (gam) to identify spatially congruent phylogeographic breaks among marine species (as areas of high BGF frequency occurrence). Lm identified a significant negative correlation between the occurrence of BGF and latitude, suggesting that population in the tropics are genetically more structured than in higher latitudes. This result bears strong association with the latitude species diversity gradient observed worldwide. Gam identified Cape São Roque (05° 28’ S) as the main BGF for populations with continuous distribution along the Brazilian coast. Cape São Roque is located near the center point region where the South Equatorial Current splits into the northward North Brazil Current and the southward Brazil Current. This study represents the first literature synthesis of Brazil’s marine phylogeography and provides a novel explicit quantitative approach to comparative phylogeography.
A key step in understanding the genetic basis of different evolutionary outcomes (e.g., adaptation) is to determine the roles played by different mutation types. To do this we must simultaneously consider different mutation types in an evolutionary framework. Here we propose a research framework that directly utilizes the most important characteristics of mutations, their population genetic effects, to determine their relative evolutionary significance. We review known population genetic effects of different mutation types and show how these may be connected to different evolutionary outcomes. We provide examples of how to implement this framework and pinpoint areas where more data, theory and synthesis are needed. Linking experimental and theoretical approaches to examine different mutation types simultaneously is a critical step towards understanding their evolutionary significance.
Telomere length is increasingly used as a biomarker of long-term life history costs, ageing and future survival prospects. Yet, to have the potential to predict long-term outcomes, telomere length should exhibit a relatively high within-individual repeatability over time, which has been largely overlooked in past studies. To fill this gap, we conducted a meta-analysis on 74 studies reporting longitudinal telomere length assessment in non-mammalian vertebrates, with the aim to establish the current pattern of within-individual repeatability in telomere length and to identify the methodological (e.g. qPCR/TRF, study length) and biological factors (e.g. taxon, wild/captive, age class, species lifespan, phylogeny) that may affect it. While the median within-individual repeatability of telomere length was moderate to high (R = 0.55; 95% CI: 0.05-0.95; N = 82), marked heterogeneity between studies was evident. Measurement method affected strongly repeatability estimate, with TRF-based studies exhibiting high repeatability (R = 0.80; 95% CI: 0.34-0.96; N = 25), while repeatability of qPCR-based studies was only half of that and more variable (R = 0.46; 95% CI: 0.04-0.82; N = 57). While phylogeny explained some variance in repeatability, phylogenetic signal was not significant (λ = 0.32; 95% CI: 0.00-0.83). None of the biological factors investigated here had a statistically significant association with the repeatability of telomere length, being potentially obscured by methodological noise. Our meta-analysis highlights the need to carefully evaluate and consider within-individual repeatability in telomere studies to ensure the robustness of using telomere length as a biomarker of long-term survival and fitness prospects.
Germline mutations are the raw material for natural selection, driving species evolution and the creation of earth’s biodiversity. Life on earth would stagnate without this driver of genetic diversity. Yet, it is a double-edged sword. An excess of mutations can have devastating effects on fitness and population viability. It is therefore one of the great challenges of molecular ecology to determine the rate and spectrum by which these mutations accrue across the tree of life. Advances in high-throughput sequencing are providing new opportunities for characterizing these rates and patterns within species and populations, thus informing essential evolutionary parameters such as the timing of speciation events, the intricacies of historical demography, and the degree to which lineages are subject to the burdens of mutational load. Here, we will focus on the applications and limitations of whole-genome comparisons among closely related individuals in what are typically described as “trio” analyses for the detection of germline mutations as they arise in real time. By sequencing and comparing whole-genomes generated for individuals of known relatedness – typically, parent to offspring – investigators can ideally count and characterize mutations as they appear per generation. The promise for gaining insight into classic hypotheses of molecular evolution is high, though so too is the cost. Namely, the technical challenges are daunting given that pedigree-based studies are essentially searching for needles in a haystack. Even so, the opportunities are so enticing, and the field so young, we can say with confidence that fundamental insights have only just begun to emerge.
There is ample evidence that macroscopic animals form geographic clusters termed as zoogeographic realms (zones), whereas distributions of species of microscopic animals are still poorly understood. The common view has been that micrometazoans, thanks to their putatively excellent dispersal abilities, are subject to the ‘Everything is Everywhere but environment selects’ hypothesis (EiE). One of such groups, <1 mm in length, are limnoterrestrial water bears (Tardigrada), which can additionally enter cryptobiosis that should further enhance their potential for long distance dispersion (e.g. by wind). However, an increasing number of studies, including the most recent phylogeny of a eutardigrade genus Milnesium, seem to question the general applicability of the EiE hypothesis to tardigrade species. Nevertheless, all the Milnesium phylogenies published to date were based on a limited number of populations, which are likely to falsely suggest limited geographic ranges. Thus, in order to comprehensively test the EiE hypothesis, here, we considerably enlarged the Milnesium dataset both taxonomically and geographically, and we analysed it in tandem with climate type and reproductive mode. Additionally, we time-calibrated our phylogeny to align it with major geological events. Our results show that, although cases of long distance dispersal are present, they seem to be rare and mostly ancient. Overall, Milnesium species are restricted to single zoogeographic realms, which suggests that these tardigrades have limited dispersal abilities. Finally, our results also suggest that the breakdown of Gondwana may influenced the evolutionary history of Milnesium. In conclusion, phylogenetic relationships within the genus seem to be determined mainly by paleogeography.
Climate change causes upward shift of forest lines worldwide, with consequences on soil biota and carbon (C). Using a space-for-time approach, we analyse compositional changes in the soil biota across the forest line ecotone, an important transition zone between different ecosystems. We collected soil samples along transects stretching from subalpine mountain birch forests to low-alpine vegetation. Soil fungi and micro-eukaryotes were surveyed using DNA metabarcoding of the 18S and ITS2 markers, while ergosterol was used to quantify fungal biomass. We observed a strong shift in the soil biota across the forest line ecotone: Below the forest line, there were higher proportions of basidiomycetes and mucoromycetes, including ectomycorrhizal and saprotrophic fungi. Above, we observed relatively more root-associated ascomycetes, including Archaeorhizomycetes, ericoid mycorrhizal fungi and dark septate endophytes. Ergosterol and percentage C content in soil strongly and positively correlated with the abundance of root-associated ascomycetes. The predominance of ectomycorrhizal and saprotrophic fungi below the forest line likely promote high C turnover, while root-associated ascomycetes above the forest line may enhance C sequestration. With further rise in forest lines, there will be a corresponding shift in the belowground biota linked to C sequestration processes.
Reconstructing the geographic origins of invasive species is critical for establishing effective management strategies. Frequently, molecular investigations are undertaken when the source population is not known, however; these analyses are constrained both by the amount of diversity present in the native region and by changes in the genetic background of the invading population following bottlenecks and/or hybridization events. Here we explore the geographical origins of the invasive winter moth (Operopthera brumata L.) that has caused widespread defoliation to forests, orchards, and crops in four discrete regions: Nova Scotia, British Columbia, Oregon, and the northeastern United States. It is not known whether these represent independent introductions to North America, or “stepping stone” spread among regions. Using a combination of Bayesian assignment and approximate Bayesian computation methods, we analyzed a population genetic dataset of 24 polymorphic microsatellite loci. We estimate that winter moth was introduced to North America on at least four occasions, with the Nova Scotian and British Columbian populations likely being introduced from France and Sweden, respectively; the Oregonian population likely being introduced from either the British Isles or northern Fennoscandia; and the population in the northeastern United States likely being introduced from somewhere in Central Europe. To our surprise, we found that hybridization has not played a large role in the establishment of winter moth populations even though previous reports have documented widespread hybridization between winter moth and a native congener. We discuss the impact of genetic bottlenecks on analyses meant to determine region of origin.
Understanding where and how genetic variation is maintained within populations is important from an evolutionary and conservation perspective. Signatures of past selection suggest that pathogen-mediated balancing selection is a key driver of immunogenetic variation, but studies tracking contemporary evolution are needed to help resolve the evolutionary forces and mechanism at play. Previous work in a bottlenecked population of Seychelles warblers (Acrocephalus sechellensis) show that functional variation has been maintained at the viral-sensing Toll-like receptor 3 (TLR3) gene. Here, we characterise evolution at this TLR3 locus over a 25-year period within the original remnant population of the Seychelles warbler, and in four other derived, contained populations. Results show a significant and consistent temporal decline in the frequency of the TLR3C allele in the original population, and that similar declines in the TLR3C allele frequency occurred in all the derived populations. Individuals (of both sexes) with the TLR3CC genotype had lower survival, and males - but not females - that carry the TLR3C allele had significantly lower lifetime reproductive success than those with only the TLR3A allele. These results indicate that positive selection, caused by an as yet unknown agent, is driving TLR3 evolution in the Seychelles warblers. No evidence of heterozygote advantage was detected. However, whether the positive selection observed is part of a longer-term pattern of balancing selection (through fluctuating selection or rare-allele advantage) cannot be resolved without tracking the TLR3C allele in the populations over an extended period of time.
Comprising more than 1400 species, bats possess adaptations unique among mammals including powered flight, unexpected longevity given small body size, and extraordinary immunity. Some of the molecular mechanisms underlying these unique adaptations includes DNA repair, metabolism and immunity. However, analyses have been limited to a few divergent lineages, reducing the scope of inferences on gene family evolution across the Order Chiroptera. We conducted an exhaustive comparative genomic study of 37 bat species encompassing a large number of lineages, with a particular emphasis on multi-gene family evolution across immune system and metabolic genes. In agreement with previous analyses, we found lineage-specific expansions of the APOBEC3 and MHC-I gene families, and loss of the proinflammatory PYHIN gene family. We inferred more than 1,000 gene losses unique to bats, including genes involved in the regulation of inflammasome pathways such as epithelial defense receptors, the natural killer gene complex and the interferon-gamma induced pathway. Gene set enrichment analyses revealed genes lost in bats are involved in defense response against pathogen-associated molecular patterns and damage-associated molecular patterns. Gene family evolution and selection analyses indicate bats have evolved fundamental functional differences compared to other mammals in both innate and adaptive immune system, with the potential to enhance anti-viral immune response while dampening inflammatory signaling. In addition, metabolic genes have experienced repeated expansions related to convergent shifts to plant-based diets. Our analyses support the hypothesis that, in tandem with flight, ancestral bats had evolved a unique set of immune adaptations whose functional implications remain to be explored.
By studying invasive species, evolutionary geneticists have been able to simultaneously inform management strategies and quantify rapid evolution in the wild. The role of genomics in invasion science is increasingly recognised, and the growing availability of reference genomes for invasive species is paving the way for whole-genome resequencing studies in a wide range of systems. Here, we survey the literature to assess the application of whole-genome resequencing data in invasion biology. For some applications, such as the reconstruction of invasion routes in time and space, sequencing the whole genome of many individuals simply increases the accuracy of existing methods. In other cases, population genomic approaches such as haplotype analysis can permit entirely new questions to be addressed and new technologies to be applied. To date whole-genome resequencing has only been applied to a handful of invasive systems, but these studies have highlighted important roles for processes such as balancing selection and hybridization that allow invasive species to reuse existing adaptations and rapidly overcome the challenges of a foreign ecosystem. The use of genomic data does not constitute a paradigm shift per se, but by leveraging new theory, tools, and technologies, population genomics can provide unprecedented insight into basic and applied aspects of invasion science.
In a recent paper, “Environmental DNA: What’s behind the term? Clarifying the terminology and recommendations for its future use in biomonitoring”, Pawlowski et al. argue that the term eDNA should be used to refer to the pool of DNA isolated from environmental samples, as opposed to only extra-organismal DNA from macro-organisms. We agree with this view. However, we are concerned that their proposed two-level terminology specifying sampling environment and targeted taxa is overly simplistic and might hinder rather than improve clear communication about environmental DNA and its use in biomonitoring. Not only is this terminology based on categories that are often difficult to assign and uninformative, but it ignores what is in our opinion the most important distinction within eDNA: the type of DNA (organismal or extra-organismal) from which ecological interpretations are derived.
Reproductive isolation is often achieved when genes that are neutral or beneficial in their genomic background become functionally incompatible in a foreign genome, causing inviability, sterility or low fitness in hybrids. Recent studies suggest that mitonuclear interactions are among the initial incompatibilities to evolve at early stages of population divergence across taxa. Yet, it is unclear whether mitonuclear incompatibilities involve few or many regions in the nuclear genome. We employ an experimental evolution approach starting with unfit F2 interpopulation hybrids of the copepod Tigriopus californicus, in which compatible and incompatible nuclear alleles compete in a fixed mitochondrial background. After about nine generations, we observe a generalized increase in population size and in survivorship, suggesting efficiency of selection against maladaptive phenotypes. Whole genome sequencing of evolved populations showed some consistent allele frequency changes across the three replicates of each reciprocal cross, but markedly different patterns between mitochondrial background. In only a few regions (~6.5% of the genome), the same parental allele was overrepresented irrespective of the mitochondrial background. About 33% of the genome shows allele frequency changes consistent with divergent selection, with the location of these genomic regions strongly differing between mitochondrial backgrounds. The dominant allele matches the mitochondrial background in 87 and 89% of these genomic regions, consistent with mitonuclear coadaptation. These results suggest that mitonuclear incompatibilities have a complex polygenic architecture that differs between populations, potentially generating genome wide barriers to gene flow between closely related taxa.
Wildlife species are challenged and threatened by various infectious diseases that act as important selective forces and demographic drivers of populations. Yet, studies about host genetic factors and disease susceptibility are very limited. Cetacean morbillivirus (CeMV) has emerged as a major viral threat to cetacean populations worldwide, contributing to the death of tens of thousands of individuals of multiple dolphin and whale species. To understand the genomic basis of immune responses to CeMV, we generated and analysed whole genomes of 53 Indo-Pacific bottlenose dolphins (Tursiops aduncus) exposed to Australia’s largest CeMV-related mortality event known to date. The genomic dataset consisted of 7,720,686 SNPs anchored onto 23 chromosome-length scaffolds and 77 short scaffolds. Allele frequency estimates between survivors and non-survivors of the outbreak revealed 11,009 candidate SNPs, of which 498 were annotated to 220 protein coding genes. These included 36 genes with functions related to innate and adaptive immune responses, and cytokine signalling pathways. The list also included genes known to be involved in immune responses to other morbilliviruses, such as measles in humans and the phocine distemper virus in pinnipeds. Our study characterised genomic regions and pathways that likely contribute to CeMV susceptibility and resistance in dolphins, representing a stride towards clarifying the complex interactions of the cetacean immune system. It also emphasises the relevance of whole genome datasets to study the genetics of wildlife diseases.
Biological invasions are accelerating, and invasive species can have large economic impacts as well as severe consequences for biodiversity. During invasions, species can interact, potentially resulting in hybridization. Here, we examined two Cakile species, C. edentula and C. maritima (Brassicaceae), that co-occur and may hybridize during range expansion in separate regions of the globe. Cakile edentula invaded each location first, while C. maritima established later, apparently replacing the former. We assessed the evidence for hybridization in western North America and Australia, where both species have been introduced, and identified source populations with 4561 SNPs using Genotype-by-Sequencing. Our results indicate that the C. edentula in Australia originated from one region of eastern North America while in western North America it is likely from multiple sources. The C. maritima in Australia were derived from at least two different parts of Europe while the introduction in western North America is from one. Although morphological evidence of hybridization is generally limited to mixed species populations in Australia and virtually absent elsewhere, our genetic analysis revealed relatively high levels of hybridization in Australia (58% hybrids) and supported the presence of hybrids in western North America (16%) and New Zealand. Hybrids might be commonly overlooked in invaders, as identification based solely on morphological traits may represent only the tip of the iceberg. Our study reveals a repeated pattern of invasion, hybridization and apparent replacement of one species by another, which offers an opportunity to investigate the role of hybridization and introgression during invasion.