The blue shark Prionace glauca is a top predator with one of the widest geographic distributions of any shark species, yet classified as critically endangered in the Mediterranean Sea, and Near Threatened globally. Previous genetic studies did not reject the null hypothesis of a single global population across the worldwide species range. Blue shark situation was proposed as a possible archetype of the ‘grey zone of population differentiation’, coined to designate cases where population structure may be too recent or too faint to be detected using a limited set of markers. Here, blue shark samples collected throughout its global range were sequenced using a specific ddRAD method (DArTseq; Georges et al. 2018), which recovered 37,655 genome-wide single nucleotide polymorphisms (SNPs). Two main groups emerged, with Mediterranean Sea and Northern Atlantic samples significantly differentiated from the Indo-west Pacific samples. Significant pairwise FST values indicated further genetic differentiation within the Atlantic Ocean, and between the Atlantic Ocean and the Mediterranean Sea. Reconstruction of recent demographic history suggested the divergence between northern and southern oceanic populations emerged about 500 generations ago and revealed a drastic reduction in effective population size from a large ancestral population. Our results illustrate the power of high-density genome scans to detect population structure and reconstruct demographic history in highly migratory marine species. As the management of the blue shark fishery, either as target or as bycatch, does not account for this delineation, we strongly recommend that the results presented here be considered in future stock assessment and management plans.
Pollination is a key step of plant reproduction, allowing individual plants to produce offspring as father, mother or both. However, few studies exist that consider together male and female pollination success. This implies studying both mating system, through paternity analyses, and seed set, by measuring the percentage of flowers giving a seed. Studying these two processes together is needed as they are not independent: gaining fitness advantage through one sex can incur fitness costs through the other due to various tradeoffs including direct sexual interference. Hence, we developed the first spatially explicit mixed-mating model integrating these two interactive processes, by coupling a mating model with a fruit set model, therefore jointly exploring pollen export and import. We used as model an insect-pollinated tree species, chestnut. We carried out a paternity analysis based on nearly exhaustive sampling of potential pollen donors in an intensively studied plot of 273 trees belonging to three interfertile chestnut species and including both male-fertile and male-sterile individuals. We collected a large dataset of 1924 mating events. We further performed fruit set measurements for 216 trees. Our process-based model predicts fruit set with great accuracy, but only if we account for self-pollen interference and associated ovule discounting, a form of sexual interference. This model represents an important step forward for fundamental pollination studies aiming at comprehensively exploring pollen emission, transport and reception in a single study, thus clarifying the consequences of pollination on male and female fitness.
Insects often harbor heritable symbionts that provide defense against specialized natural enemies, yet little is known about symbiont protection when hosts face simultaneous threats. In pea aphids (Acyrthosiphon pisum), the facultative endosymbiont Hamiltonella defensa confers protection against the parasitoid, Aphidius ervi, and Regiella insecticola protects against aphid-specific fungal pathogens, including Pandora neoaphidis. Here we investigated whether these two common aphid symbionts protect against a specialized virus A. pisum virus (APV), and whether their anti-fungal and anti-parasitoid services are impacted by APV infection. We found that APV imposed large fitness costs on symbiont-free aphids and these costs were elevated in aphids housing H. defensa. In contrast, APV titers were significantly reduced and costs to APV infection were largely eliminated in aphids with R. insecticola. To our knowledge, R. insecticola is the first aphid symbiont shown to protect against a viral pathogen, and only the second arthropod symbiont reported to do so. In contrast, APV infection did not impact the protective services either R. insecticola or H. defensa. To better understand APV biology, we produced five genomes and examined transmission routes. We found that moderate rates of vertical transmission, combined with horizontal transfer through food plants, were the major route of APV spread, although lateral transfer by parasitoids also occurred. Transmission was unaffected by facultative symbionts. In summary, the presence and species identity of facultative symbionts resulted in highly divergent outcomes for aphids infected with APV, while not impacting defensive services that target other enemies. These findings add to the diverse phenotypes conferred by aphid symbionts, and to the growing body of work highlighting extensive variation in symbiont-mediated interactions.
Any random genetic change is more likely to impair than improve fitness, a situation that owes to the fact that contemporary genotypes bear a history of having been shaped by natural selection for a very long time. Most mutations are thus deleterious and generate a genetic load that can be difficult to handle in small populations and increase the risk of extinction. We used functional annotation and evolutionary conservation scores to study deleterious variation in 200+ genomes from the highly inbred Scandinavian wolf population, founded by only three wolves and suffering from inbreeding depression, and neighboring populations in northern Europe. The masked load was high in Russia and Finland with deleterious alleles segregating at lower frequency than neutral variation. Genetic drift in the Scandinavian population led to the loss of ancestral alleles and fixation of deleterious variants. The per-individual realized load increased with the extent of inbreeding and reached several hundred homozygous deleterious genotypes in protein-coding genes, and a total of more than 50,000 homozygous deleterious genotypes in the genome. Arrival of immigrants gave a temporary genetic rescue effect with ancestral alleles re-entering the population and moving deleterious alleles into heterozygote genotypes. However, in the absence of permanent connectivity inbreeding has then again led to the exposure of deleterious mutations. These observations provide genome-wide insight into the character of genetic load and genetic rescue at the molecular level, and in relation to population history. They emphasize the importance of securing gene flow in the management of endangered populations.
The term “haplotype block” is commonly used in the developing field of haplotype-based inference methods. We argue that the term should be defined based on the structure of the Ancestral Recombination Graph (ARG), which contains complete information on the ancestry of a sample. We use simulated examples to demonstrate key features of the relation between haplotype blocks and ancestral structure, emphasising the stochasticity of the processes that generate them. Even the simplest cases of neutrality or of a “hard” selective sweep produce a rich structure, which is missed by commonly used statistics. We highlight a number of novel methods for inferring haplotype structure as full ARG, or as a sequence of trees. While some of these new methods are computationally efficient, they still lack features to aid exploration of the haplotype blocks, as we define them, thus calling for the development of new methods. Understanding and applying the concept of the haplotype block will be essential to fully exploit long and linked-read sequencing technologies.
Community-level traits as a way to partly circumvent the culturing problem in mycorrhizal trait-based ecology?Chagnon, P.-L.Data availability statement: No new data has been generated in this manuscript.Traits are the intermediate by which species respond to environmental filters and influence ecosystem functions. With the myriad of biogeochemical processes controlled by fungi, the past decade has witnessed a rising interest in applying trait-based approaches, core to the toolkit of plant and animal ecophysiologists, to fungi. One of the first challenges to tackle when working on fungal ecophysiology is to circumscribe the very definition of what we consider a fungal trait. Traits are characteristics/features possessed by an individualthat can influence how it interacts with its environment. Here the individual scale is both important, and problematic. Important because the very goal of comparative ecology is to measure traits on individuals belonging to known species. This allows to populate trait databases, and syntheses of such databases can reveal key trade-offs and trait syndromes that govern species’ life-histories. The scale of the individual is problematic, however, because it is hard to define for soil fungi, and because a rare minority of fungi can be sampled at the individual scale in the environment (e.g., macroscopic sporocarps, ectomycorrhizal root tips, lichen thalli). Beyond this minority, the individual organisms can only be accessed/sampled through establishing fungal cultures, which probably represents one of the main bottlenecks in the development of fungal trait databases. In this issue, Zhang et al. (2022) show how interesting insights in fungal trait-based ecology can be gained by working at the community level.In their study, Zhang et al. (2022) adapted a protocol developed by Neumann & George (2005) to capture mycorrhizal fungal hyphae using ingrowth bags. If we assume that most hyphae recovered through this technique are mycorrhizal, the washed hyphae can be characterized through various chemical/morphological downstream analyses. Measuring such traits for biomass recovered from whole communities is akin to estimating community-weighted mean (CWM) traits, which are central to many aspects of ecophysiology. Various paradigms/theories in community ecology assume some form of equilibrium between species and their environment (Leibold et al., 2004). If we assume (1) a heterogeneous environment, (2) species as reproductively isolated units competing for space/resources and (3) traits as determinants of their reproductive success, correlations between species traits and environmental parameters are naturally expected to arise (Shipley et al., 2011). Under specific stable environmental conditions, a species bearing certain traits should have a higher probability to (1) occur and (2) become abundant in such environment. At the community level, we thus expect a correlation between CWM traits (the sum of species mean traits weighted by their relative abundances), and environmental parameters (box 1). With mycorrhizal fungi, we can have a reasonable access to species’ relative abundances through sequence-based profiles of communities, but the species × traits matrix remains inaccessible. The shortcut taken by Zhang et al. (2022) is to take measurements of traits (here, hyphal C:N:P stoichiometry) at the community level directly.Does the species × traits become dispensable in mycorrhizal ecology? Certainly not. Bringing mycorrhizal fungi into cultures, identifying traits likely to represent important trade-offs in fungal resource management strategies (Chagnon et al., 2013), ensuring reproducible measurement of such traits and establishing common resources to share such traits (Kattge et al., 2020; Zanne et al., 2020) remains a priority of mycorrhizal ecophysiology. Opinions (Chagnon et al., 2013) and definitions (Chaudhary et al., 2020) will only be useful if followed by actual work to populate databases currently storing the very fragmentary data on fungal traits. We cannot leave aside this important work at the species and individual scales, because evolutionary trade-offs defining resource management and life history strategies emerge at those very scales, not at the community level (Grime & Pierce, 2012).Trait-environment relationships, however, can inform us on the way environmental pressures may select for particular species characteristics, and in this regard, progress can be made over much shorter timescales than the work expected to rely on permanent culture banks and individual-level trait measurements. Zhang et al. (2022), for example, identified an increase in hyphal P concentrations in response to warming and drought treatments, illustrating hyphal stoichiometry as a potentially important “response trait” for mycorrhizal fungi. The upcoming challenge with stoichiometry is now to link form and function. What is the purpose of enhanced mycelial P for the fungus? Luxury uptake and storage as polyphosphates, which may confer bargaining power to the fungus? Increased cellular concentration of “growth-related molecules” (sensu Zhang et al., 2022) such as RNA? This remains to be elucidated. The same is true for nitrogen, which can be present in both growth- and function-related proteins, or in cell wall components slowing down necromass decomposition (Fernandez et al., 2019). This will influence how likely are fungal hyphae to contribute to soil organic pools of different turnover times (See et al., 2022; Klink et al., 2022).We can probably identify many other traits that we expect to be (1) measurable at the community level and (2) associated with environmental filters. Spore size and wall ornamentations could be linked to dispersal dynamics (e.g., Chaudhary et al., 2020). Cell wall thickness could be linked with susceptibility to fungivory (as a constitutive structural defense), and could be expected to be associated with predation risk, but also community-level productivity. Generally, structural defenses are expected to be maximal under harsh conditions promoting conservative species with long-lived, constitutively defended tissues (Coley, 1988). Hyphal allocation allometry to the root vs. the soil habitats already has received considerable attention (e.g., Maherali & Klironomos, 2007), although the assumption that extensive soil foraging is associated with more efficient P return to host can be questioned (Jakobsen et al., 1992). Community-level allometric measurements could be coupled with soil nutrient availability along natural or experimental gradients could clarify this issue. Relative mycelial investments in the soil, however, is a multifaceted trait that bears implication for other aspects of fungal growth and dispersal, namely the colonization of new patches (emerging roots), the exposition to parasites/predators, and the interactions with non-mycorrhizal microorganisms potentially including hyphosphere mutualists. In other words, soil hyphae are not strictly foraging units, but may also serve dispersal, chemical warfare and interkingdom cooperation. This may decrease the probability of finding clear univariate linkages between hyphal allometry and single environmental filters such as nutrient availability. Other traits requiring our attention are biomass growth and turnover rates. Tissue maximal growth rate and lifespan are central to the definition of ecological strategies (e.g., Westoby et al., 2002; Darling et al., 2012). In principle, this can be measured at the community level for mycorrhizal fungi, although the experimental approach should be selected wisely. Traditional approaches to measuring biomass accumulation in mycorrhizal studies typically rely either on microcosms inoculated with fungal propagules, or on ingrowth bags. Both these approaches will select for colonists that can rapidly invade this new empty niche (a bulk sterile pot/ingrowth bag), thus biasing our estimates of growth rates in favor of those displayed by ruderal colonists (i.e., community-level trait not matching the community composition/structure). However, regarding biomass turnover rates, it could be envisaged to derive such estimate using stable isotope probing targeting a specific biomarker (e.g., NLFA 16:1ω5). The only drawback is that evaluating dilution rate of heavy carbon in such a biomarker rapidly makes the cost per sample prohibitive, hampering measurements of biomass turnover rates along environmental gradients, or in response to an experimental treatment.Despite the technical difficulties associated with measuring community-level traits, or the challenges to linking form and function, the approach put forth by Zhang et al. (2022) with hyphal stoichiometry are part of the equation to advance mycorrhizal ecophysiology, and should be extended to other traits. Meanwhile, the long-term objective for mycorrhizal ecophysiologists should still be to isolate and culture strains, and make these permanent resources for them and other research groups to measure traits in future studies. Intraspecific trait variation appears so important, at least for arbuscular mycorrhizal fungi (e.g., Munkvold et al., 2004; Antunes et al., 2011), that strain identity will be just as important as species identity in building trait databases. And as mycorrhizal ecophysiology matures, new traits will gain interest and have to be measured on those strains for which we have already measured a number of other traits. Plant and animal ecophysiologists have a permanent resource they can sample individuals from: it is called nature. Mycorrhizal ecologists are in need for such analogous resource: permanent culture banks. Thus, it seems that challenges lying ahead in mycorrhizal ecophysiology are multifaceted, encompassing the need for conceptual development, standard laboratory methods, but also creativity in getting long-term funding to maintain biological material.
Invasive species can successfully and rapidly colonize new niches and expand ranges via founder effects and enhanced tolerance towards environmental stresses. However, the underpinning molecular mechanisms (i.e., gene expression changes) facilitating rapid adaptation to harsh environments are still poorly understood. The red seaweed Gracilaria vermiculophylla, which is native to the northwest Pacific but invaded North American and European coastal habitats over the last 100 years, provides an excellent model to examine whether enhanced tolerance at the level of gene expression contributed to its invasion success. We collected G. vermiculophylla from its native range in Japan and from two non-native regions along the Delmarva Peninsula (Eastern United States) and in Germany. Thalli were reared in a common garden for four months at which time we performed comparative transcriptome (mRNA) and microRNA (miRNA) sequencing. MRNA-expression profiling identified 59 genes that were differently expressed between native and non-native thalli. Of these genes, most were involved in metabolic pathways, including photosynthesis, abiotic stress, and biosynthesis of products and hormones in all four non-native sites. MiRNA-based target-gene correlation analysis in native/non-native pairs revealed that some target genes are positively or negatively regulated via epigenetic mechanisms. Importantly, these genes are mostly associated with metabolism and defense capability. Thus, our gene expression results indicate that resource reallocation to metabolic processes is most likely a predominant mechanism contributing to the range-wide persistence and adaptation of G. vermiculophylla in the invaded range. This study therefore provides a novel molecular insight into the speed and nature of invasion-mediated rapid adaption.
Integrating telomere biology into the ecology and evolution of natural populations: progress and prospectsMonaghan, Pat1; Olsson, Mats2; Richardson, David S.3; Verhulst, Simon4; and Rogers, Sean M.5,6,*1. Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow Glasgow, G12 8QQ, UK.2. Department of BioEnv – Zoologen, University of Gothenburg, Sweden3. School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, Norfolk NR4 7TJ, UK4. Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands.5. Department of Biological Sciences, University of Calgary, Calgary, Canada6. Bamfield Marine Sciences Centre, Bamfield, Canada* corresponding authorOrcid Id:Simon Verhulst: 0000-0002-1143-686Pat Monaghan: 0000-0003-2430-0326Mats Olssen; 0000-0002-4130-1323Sean M Rogers; 0000-0003-0851-8050David S Richardson: 0000-0001-7226-9074Telomeres are fascinating stretches of protective DNA that cap the chromosome ends of eukaryotes. Without telomeres, during cell division and DNA replication, DNA repair proteins would misread the ends of chromosomes and attempt to repair or remove this region of the genome, leading to instability. Furthermore, the loss of DNA that inevitably occurs during cell replication due to the end replication problem and oxidative damage would erode the coding sequences of chromosomes, eventually causing genome malfunction. Telomeres protect the chromosome, but in the absence of restoration, some reduction in telomere length will occur with each cell division, eventually giving rise to cell replicative senescence often followed by cell death. Short and/or dysfunctional telomeres underly many disease states and are associated with ageing. Consequently, telomere biology is a vibrant area of biomedical research. However, until relatively recently, most of the research on telomeres has been focused on humans or animal models. That the basic pattern of progressive telomere loss and little restoration in most somatic tissues, as found in humans, might not apply to all eukaryotes had received relatively little attention. In fact, any variation in the expected pattern of decline in chromosomal telomere length with progressive rounds of cell replication, as observed in most human tissues, was initially attributed to methodological issues. Importantly, the science of studying telomeres has now expanded to encompass non-model organisms. Variation in the pattern of telomere loss and restoration across a range of species promises to reveal great insights into the drivers of life-history trade-offs and evolution, population ecology and consequences of exposure to environmental stress in natural populations.The burgeoning interest in telomere dynamics in non-model organisms and increased communication between biomedical researchers and evolutionary ecologists is now enriching our understanding of the diversity of telomere dynamics. While the basics of telomere biology appear to be conserved across the eukaryotes, and the range of species studied is still phylogenetically restricted, differences in detail are increasingly being revealed (Monaghan et al. 2018). We now have information on how the pattern of telomere change can vary among species and include lengthening as well as shortening across the life course (Remot et al 202x, Brown et al. 2022). Our understanding of how these patterns relate to environmental factors, species, individual histories and population process is increasing. Furthermore, telomere biology has the potential to be used in conservation biology, providing information about individual and population health (e.g. Eastwood et al. 2022). The molecular ecology of telomeres in non-model organisms will have greater impact as discoveries will increase our understanding of the genomics, ecology and evolution underlying telomere diversity. This special issue brings together a collection of papers that illustrate the breadth of taxa now being investigated and ways in which emerging hypotheses, formed from the perspectives of ecology, evolution and conservation, are being tested. In this introduction, we highlight how this body of work, including new information and insights, points the way to many research questions that remain to be investigated in this emerging, cross-disciplinary area of biology.Ecological and environmental stressorsExposure to stressful environments can have long lasting effects on health and longevity, and some of these effects are linked to changes in telomere dynamics. In addition to furthering our understanding of the mechanism underlying these adverse effects, the study of telomere dynamics in relation to environmental conditions offers the potential to measure the scale and extent of their impact at individual and population levels (Kärkkäinen et al 202xa), evaluate environmental quality and examine the effect of conservation measures, such as habitat restoration. In this special issue, Brown et al. 2021 report apparent telomere lengthening in both sexes associated with increased survival in a small passerine bird, the Seychelles warbler Acrocephalus sechellensis . However, sex-specific effects of stressors influenced the patterns of telomere change. In females, stress induced by low food availability and malarial infection was associated with the expected telomere shortening, but there were no such effects in males. Moreover, less exposure to such stresses appeared to lead to telomere lengthening (Brown et al 2021). Reichard et al. (2021) also report intraspecific variation in the outcome of stress exposure using African killifish. This involves strains derived from wild populations ofNothobranchius furzeri and its sister species, N. kadleci , from sites along a strong gradient of aridity, which ultimately determines maximum natural lifespan in these species. Interestingly, they demonstrate that individual condition and environmentally-driven selection can modulate the relationship between telomere length and lifespan in opposite directions, validating the existence of inverse trends within a single taxon and again highlighting the importance of sex-specific effects. Altogether, the apparent association between telomere lengthening and stress exposure (see below for further examples) and among individual differences in telomere dynamics, for example in relation to age, sex or individual history, require further investigation. Such studies need to use accurate and repeatable within-individual measurements where possible and bear in mind the need to take measurement error into account (Steenstrup et al. 2013).Intrinsic and extrinsic stress exposures in early life are known to have substantial and long-lasting effects on phenotypic development. Conditions experienced inside the cell or from the external environment during growth can influence telomere dynamics, as shown in this special issue. In European badgers Meles meles , van Lieshout et al. (2021) report that cubs born in warmer, wetter springs have longer telomere lengths, which is in turn linked to survival. In purple-crowned fairy wrens (Malurus coronatus ) the rate of telomere shortening in the first year of life predicted lifespan (Sheldon et al 2021b). More broadly, it has been hypothesized that measuring the effects of adverse environmental conditions induced by anthropogenic stressors (such as chemical pollutants, noise and inappropriate light) on telomere dynamics could assist in the monitoring and conservation of wildlife. In this context telomere measurements have the potential advantage over many other biomarkers of representing a potential fitness proxy, allowing effects to be studied over a time scale that could be much shorter than required to measure actual fitness consequences. In line with this, Salmón and Burraco (2022) evaluated the use of changes in telomere dynamics as a way of assessing such anthropogenic impacts, providing an exhaustive literature review and meta-analysis. Oxidative stress induced by internal and external factors can be a major cause of DNA damage which could increase telomere attrition. Metcalfe and Olsson (2021) provide a compelling case that endogenous reactive oxygen species produced in the mitochondria create links between mitochondrial function, DNA integrity and telomere dynamics. They argue that telomere dynamics are best understood when considering the optimal solution to the trade-off between energetic efficiency and chromosomal protection that will differ among individuals and change over time, depending on resource availability, energetic demands and life history strategy. Such inferences may cumulatively help explain why the effects of stressors on telomere dynamics are evident (but apparently also stressor, taxon, and sometimes sex-specific). Clearly the research directions proposed in this special issue will contribute to a better understanding of these mechanisms that link environment, lifestyle and telomere dynamics.At present, telomere research on non-model organisms has been primarily focused on the endothermic vertebrates - birds and mammals. Nucleated red blood cells are primarily used in bird studies while white blood cells are most often in mammals, particularly humans. Thus, tissue specificity in telomere dynamics associated with these cell types may itself underlie some of the differences reported. However, the majority of animals are ectotherms and often differ from many endotherms by having telomerase production in somatic tissues. Furthermore, many aspects of ectotherm development and performance are linked to environmental temperature, and are, therefore, potentially significantly affected by climate disruption. Friesen et al. (2021) suggest that developing thermal performance curves for the processes affecting telomere dynamics could assist in monitoring climate impacts, highlighting the pressing need for more experimental work in this area to isolate the causes of environmentally induced changes in telomere dynamics. Rouan et al. (2021) present such an experimental study on the coral, Stylophora pistillata , in which bleaching, the devastating loss of symbionts that can results from climate change, was induced by continuous darkness. This resulted in increased telomere loss. As well as telling us something about the damaging effects, these findings could inform methods for monitoring coral reef health. In a field experiment using young salmon Salmo salar , in freshwater streams, McLennan et al. (2021) found that both a lack of suitable substrate and living at high density were associated with reduced telomere length. However, in streams in which nutrient levels were experimentally restored, these adverse effects on telomere length were greatly reduced, demonstrating the potential utility of changes in telomere length in a conservation context. Further, the experiment presented by Bae et al. (2021) revealed that the effects of temperature can be influenced by interactions with pollutants. This appears to be especially prevalent in species with temperature-dependent sex determination, such as the American alligatorAlligator mississippiensis . Here the effect of experimental exposure to an endocrine disrupting chemical depended on the environmental temperature; at temperatures promoting female development, the effect on telomere length was positive, while at the higher, male promoting temperature, the effect was negative. On the other hand, raising crickets at different temperatures, which strongly affected their growth, did not significantly affect their telomere dynamics Boonekamp et al. (2021). Much may depend on how severely the potential stressor is perceived by the organism in question.In a somewhat different context, but still potentially linked to differences in stress exposure, a non-experimental study by Wood et al. (2021) used extensive longitudinal assessments of within-individual rates of change in telomere length to investigate the impacts of dominance status on telomere dynamics in the cooperative breeder, the white-browed sparrow-weaver Plocepasser mahali . They found that social dominance and rainfall predicted telomere dynamics. Looking at mechanistic processes in more detail, Wolf et al. (2021) provided novel insight into the telomere dynamics of a natural system of tree swallowsTachycineta bicolor , reporting lower expression of the telomere regulatory gene POT1 in female breeders of higher quality. They also reported that experimentally induced stress exposure in chicks induced lower POT1 expression and telomere lengthening.Collectively, these studies show that variation in stress exposure and individual resilience can contribute to intra-specific differences in telomere dynamics. They highlight the need to consider the biology of the species (including sex differences), the local conditions to which it has been exposed, what different levels of temperature change mean in terms of stress exposure for different species and populations, and the need to examine interacting environmental effects in natural populations. They also highlight that examining telomere dynamics in relation to differential expression of relevant genes in relation to ecological and environmental variables could potentially be of great interest.Telomeres and life history trade-offsMuch of the interest in telomeres from ecologists relates to their potential in mediating life history trade-offs. For example, is increased telomere damage traded off against potential advantages of larger size or greater energy expenditure? The outcome of such trade-offs may be influenced by individual state. Such state-dependent relationships are difficult to measure but variation in telomere length, or loss, might provide a relative measure. Carrying elaborate sexual ornaments is thought to be costly thereby maintaining the honesty of the signal, but little work has yet been done to test the relative cost of ornamentation using telomeres. Kauzálová et al. (2022) found that barn swallows Hirundo rustica , with long tail streamers (a sexually selected ornament (Møller 1988), have shorter telomeres. This suggests a cost to elaborate ornamentation in this species. Ravindran et al. (2021) used bivariate analysis to decompose correlations between telomere length and reproduction into within- and among individual effects. They conclude that, in wild Soay sheep Ovis aries , females had shorter telomeres in August in years in which they gave birth in spring compared to years without the gestation effort, indicative of a trade-off involving reproduction. However, at the same time in years in which they gave birth, the mother’s telomeres were longer when their lambs survived to August, compared with years when they lost their lambs earlier, suggesting complex state dependent effects. Sepp et al. (2021) conducted a cross-fostering experiment in common gulls (Larus canus ), to tease apart pre- and post-natal parental age effects on offspring telomere length. Neither the age of the natal- nor the foster parents in this study predicted the length or rate of change of telomeres in chicks.The above results are interesting, but also demonstrate that additional experimental work is needed, particularly in relation to evaluating parental state-induced telomere dynamics. A good example is provided by Atema et al. (2021) who manipulated individual state by equipping male great tits Parus major with a ‘backpack’ adding 5% to their body mass for a year. Surprisingly telomere dynamics were not affected by this extra burden, despite the duration of the experiment and large sample size. However, the absence of an effect was consistent with there being little evidence of a fitness costs of carrying this extra mass (Atema et al. 2016), information which is often lacking but critical for the interpretation of any result. In the dark-eyed junco Junco hyemalis , where experimentally elevated testosterone reduces male survival (Reed et al. 2006), elevated testosterone was also linked to accelerated telomere attrition Heidinger et al. (2021). This suggests that telomere dynamics may be part of the mechanism causing the testosterone effect on survival in this species, and that variation in state is an important issue.Trade-offs involving telomeres may also occur very early in life, for example, when resources are allocated to growth at the expense of somatic maintenance, potentially being reflected in early life telomere dynamics (Monaghan and Ozanne 2018; Vedder et al. 2018). Growth is difficult to manipulate directly and is often done through dietary manipulations, which might have confounding systemic effects that can be difficult to fully take into account. Pepke et al. (2021) examined the effect of final body size on telomere length within an artificial selection experiment on body size (tarsus length) in free-living house sparrows Passer domesticus . They studied two island populations, with selection for large body size on one island, and selection for small body size on the other. The experiment was successful in creating a difference in tarsus length between the islands - of almost 10% in the final selection year. They found a significant decrease in telomere length on the island with selection for large body size, but no change on the island with selection for small body size. The approach of Pepke et al. (2021) will hopefully be followed by others, potentially using existing selection experiments on growth and body size. Though to fully understand the results it may be important to also know more about cell division rates and growth patterns in the individuals attaining different body sizesWhile the general pattern from human studies is that telomeres shorten with age, findings in other species, including those in this special issue mentioned earlier in relation to stress exposure, suggest that this is not always the case (meta-analysed by Remot et al. 2021 in this issue). For example, there is evidence of telomere elongation in some hibernating mammals and snakes (Olsson 2018). This raises questions about the underlying mechanisms involved in telomere maintenance, with variation in telomerase activity as a likely candidate. Smith et al. (2021) review what is known about telomerase activity in ecological studies and discuss the challenges involved in measuring telomerase activity. They note that studies have not generally detected the expected link between telomere maintenance and telomerase activity, for which there can be different explanations. When telomeres are studied in blood, it is mainly the telomerase activity in the haemopoietic stem cells in the bone marrow that will affect the focal telomeres, but studying this within individuals is very difficult. Noguera et al. (2020) evaluated the effect of maternal glucocorticoids on telomerase activity in yellow-legged gulls Larus michahellis (e.g., corticosterone or cortisol) as their transmission to offspring is a potential cost associated with adverse or stressful conditions experienced by mothers. They found that egg corticosterone can stimulate telomerase activity and promote longer telomeres during embryo development, suggesting mechanistic links by which mothers may shape offspring life-history trajectories and phenotypes. In another study, Sheldon et al. (2021) tested levels of DNA methylation across early life in wild, nestling zebra finches, discovering that methylation was negatively correlated with telomere length changes, providing possible links between epigenetics and telomeres. Altogether, elucidating the ecology of gene expression and epigenetics in telomere maintenance across natural populations should therefore be considered an important task for the future.Raven et al. (2022) discuss what is known about cancer and telomeres in the wild, a topic of considerable interest since telomeres have historically been studied in the context of cancer, with somatic down-regulation of telomerase postulated as a tumour protection mechanism in large bodies/long lived species. Telomerase activation has been identified as critical mutations that are associated with malignant cells. Raven et al. (2022) emphasize that telomere-cancer dynamics constitute a complex and a multifaceted process, in part because in humans both (too) long and (too) short telomeres can be associated with an increased cancer risk. Whether similar effects can be observed in natural populations of other species remains to be seen. Telomere length predicts survival within species (Wilbourn et al. 2018), raising the question as to whether long-lived species have relatively long telomeres. Among birds, this does not appear to be the case (Tricola et al. 2018), at least when using the available estimates of maximum lifespan. In contrast, Gomes et al. (2011) reported an inverse relationship between telomere length and maximum lifespan in mammals. Pepke and Eisenberg (2021) revised and extended the data set of Gomes et al. (2011) and confirmed this inverse relationship. A possible explanation for this pattern is that short telomeres protect against cancer, because cells with short telomeres have less scope for replication before critically short telomeres induce cell replicative senescence. In line with this explanation, Pepke & Eisenberg (2021) show a positive association between telomere length and the development of neoplasia, abnormal tissue growth that can develop into malignancy. They further show that domesticated species have substantially longer telomeres than wild species with similar mass. This may be because of artificial selection of certain phenotypes, or relaxation of selection pressures in domestic species; for example domesticated animals will often be culled before reaching the natural end of their lives, diminishing selection favouring protection against the development of cancer.Heritability and EvolvabilityOne of the most remarkable aspects of telomere biology is the considerable range described for the heritability of telomere length (i.e., the parental genetic contribution additively affecting the telomere length variance in the offspring, i.e., its heritability,h2 = VA/VP). Reviews on telomere biology report perhaps the widest range in heritability of any phenotypic trait ranging from near zero to more than one (likely due to sampling error, sinceh2 cannot theoretically exceed one; Olsson et al. 2018). This makes telomere evolution difficult to reconcile with evolutionary expectations from existing quantitative genetics theory, the situation becoming more complex when the aim is to understand the potential of adaptive telomere evolution and the agents of selection. An alternative approach to using heritability for this procedure is to assess ‘evolvability’ as the expected proportional change under a unit strength of selection, yielding a mean-scaled additive variance (Houle 1992). These two measures, heritability and evolvability, have been shown to have near zero correlation, possibly due to positive correlations between the additive- and other components of the phenotypic variance (e.g., environmental-, epistatic- and dominance variance; Hansen 2011). In this special issue, aspects of quantitative genetics of telomeres and their dynamics are discussed. The main ‘other’ variance components for understanding telomere heritability, its limitations and usefulness for evolutionary inference, are epigenetic inheritance (Bauch et al. 2019), and the environmental variance (Dugdale and Richardson 2018). A straightforward expectation from theory is that when environmental variance is eliminated, heritability will be very high, which is what (Boonekamp et al. 2021; h2≈ 1) found in their laboratory experiments on field cricketsGryllus campestris . Importantly, heritability estimates are environment-specific, so to what degree these estimates predict responses to ongoing telomere selection in the wild remains to be tested. An attempt to do this in a cross-fostering experiment on jackdaws Corvus monedula , showed that heritability for telomere length was high (0.74) whereas for telomere shortening rate it was considerably lower (0.09; Bauch et al. 2021). This agrees with evolutionary theory in that telomere shortening in this taxon is more strongly correlated with components of fitness than is telomere lengthper se (Bauch et al. 2021 and references therein). Interestingly, Bauch et al.’s evolvability estimate for telomere length was only 0.48% and uncorrelated with heritability, in agreement with Hansen et al.’s evolvability review (2011). In contrast, in a study with considerably greater sample size and thus power than most QG studies on telomeres in wild animals Sparks et al. (2021) found low heritability and evolvability for telomere length in Seychelles warblers, suggesting differences may exist among species.Future DirectionsThe collection of wonderful studies in this special issue demonstrates the increasing interest in studying telomeres from an evolutionary and ecological perspective, and their potential value in areas such as conservation biology. The work reported here highlights several advances that collectively demonstrate the effect of environment on telomere dynamics and the corresponding impact on life history trade-offs and quantitative genetic consequences. In addition, the work also highlights taxonomic and conceptual areas where additional studies would benefit the field. For example, recent studies on plants have discovered that telomerase RNA homologs across the plant kingdom are structurally similar to ciliates and multicellular eukaryotes, supporting the hypothesis of a common ancestor for telomerase (Song et al. 2019) . They also provide growing evidence for the adaptive significance of plant telomeres for ecologically important traits such as flowering time (Choi et al. 2021)). However, databases on telomere traits in taxonomically diverse organisms, with variation in life histories, body sizes, growth patterns and regenerative capabilities remain limited. More work is needed on species with complex life cycles, high regenerative capacity and variable lifespans. Additional studies will hopefully enable testing of hypotheses of telomere evolutionary history, adaptive life-history strategies, and chromosomal integrity.To date, studies of telomere dynamics have benefited from long-term studies of several animal systems. There is much to be gained from the within-individual data collected from such studies and variation in population trajectories. In quantitative genetics (QG), controlling for individuals having a shared environment between generations (which inflates the heritability measure) could be achieved by cross-fostering in many various species and/or and by releasing offspring at random locations in species without parental care (Olsson et al. 2011), or by controlling for environmental ‘type’ in longitudinal studies or experimental plant and animal systems. The large samples necessary for telomere QG work can be facilitated by choice of appropriate model systems and by applying emerging techniques in molecular ecology. qPCR continues to be particularly attractive for high-throughput processing, especially in species with limited interstitial telomeres (Boonekamp et al. 2021) (Rovatsos et al. 2015; Matsubara et al. 2015). However, the potential importance of how interstitial telomere repeats influence the biology of different taxa has hardly been investigated at all (see Nussey et al. (Methods in Ecol & Evolution) for discussion of methodology). It is important that telomeres measuring methodologies are as accurate and precise as possible, while allowing for large enough sample through-put to capture variation. Avoiding problems created by selective disappearance of phenotypes is also important. Some of these issues are discussed in this special issue in reviews revealing major methodological effects on estimates of individual repeatability (Kärkkäinen et al. 202xb) and heritability (Bauch et al. 2021).A recently developed method, the single telomere absolute-length rapid (STAR) assay offers a high-throughput, digital real-time PCR approach for rapidly measuring the absolute lengths and quantities of individual telomere molecules (Luo et al. 2020) (Dwech-Maitre et al 021), although its precision remains to be evaluated. In the future the use of digital qPCR may yield higher throughput than traditional Telomere Restriction Fragment analysis (TRF) (Nussey et al 2014) and more precision than current qPCR methods. Pepke et al. (2021) examined heritability and genetic architecture using a combination of qPCR and next generation sequencing, supporting that new bioinformatic approaches using computerized telomere estimation may facilitate higher throughput and examination of non-terminal telomeres and their position effects on fitness (Nersisyan and Arakelyan 2015; Edwards 2021).Finally, many exciting questions pertaining to telomere biology in relation to ecology evolution and conservation remain to be answered. For evolutionary biologists and ecologists, variation is the ‘stuff of life’ and understanding the causes and consequences of such variation, and the role of telomeres within that is an important and exciting challenge! We still know relatively little about how flexible telomere biology is under different selection pressures and to what extent it constrains the suite of potential life histories, for example in relation to growth, body size, reproduction and lifespan. In terms of fitness, we may ask what matters most, telomere loss or telomere length? Both length and loss rate have been found to be predictive of longevity within species and much may depend on the life stage at which each is measured; it seems unlikely that limited telomere length would curtail lifespan until relatively old age, when stem cell pools are depleted and stem cells themselves show age-related deterioration. That said, telomere loss might give us a better handle on understanding stress exposure and stress resilience. In humans and birds, there is evidence that telomere length variation stabilises at the end of growth and that telomere length at this time period is the best predictor of subsequent lifespan (Benetos et al. 2013, Daniali et al. 2013, Heidinger et al 2012). Will similar patterns be revealed in species with indeterminate growth? Currently, we simply do not have the data to answer this question so much more work is needed in this area. In a conservation context, can telomere biology help us identify populations at risk from rapid environmental disruption due to anthropogenic effects, and identify species that are likely to be resilient to climate change and stress exposure? Given that the genetic basis of adaptive traits are now used to project the distribution of species in response to climate change (Wuitchik et al. 2022), it is possible that the inclusion of telomere biology may further inform and refine such projections in species distribution models.Altogether, this comprehensive collection of studies demonstrates the enormous potential for the integration of ecological and genomic approaches to continue to transform our understanding of the consequences of intrinsic and extrinsic environmental stressors and change on the ecology and evolution of natural populations. This special issue highlights how a deeper appreciation of the role of telomeres and associated properties of the genome will continue to benefit the field of Molecular Ecology.Literature CitedA.P, Møller. 1988. “Female Choice Selects for Male Sexual Tail Ornaments in the Monogamous Swallow.” Nature 332: 640–42.Atema, Els, Arie J. van Noordwijk, and Simon Verhulst. 2021. “Telomere Dynamics in Relation to Experimentally Increased Locomotion Costs and Fitness in Great Tits.” Molecular Ecology, September. https://doi.org/10.1111/mec.16162.Bae, Junsoo, Emily M. Bertucci, Samantha L. Bock, Matthew D. Hale, Jameel Moore, Phil M. Wilkinson, Thomas R. Rainwater, et al. 2021. “Intrinsic and Extrinsic Factors Interact during Development to Influence Telomere Length in a Long‐lived Reptile.” Molecular Ecology, June. https://doi.org/10.1111/mec.16017.Bauch, Christina, Jelle J. 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Trade-offs between traits arise and reflect constraints imposed by the environment and physicochemical laws. Trade-off situations are expected to be highly relevant for sessile plants, which have to respond to changes in the environment to ensure survival. Despite increasing interest in determining the genetic and molecular basis of plant trade-offs, there are still gaps and differences with respect to how trade-offs are defined, how they are measured, and how their genetic architecture is dissected. The first step to fill these gaps is to establish what is meant by trade-offs. In this review we provide a classification of the existing definitions of trade-offs according to: (1) the measures used for their quantification, (2) the dependence of trade-offs on environment, and (3) whether data based on which they are inferred are from a single individual across different environments or a population of individuals in single or multiple environments. We then compare the approaches for quantification of trade-offs based on phenotypic, between-individual, and genetic correlations, and stress the need for developing further quantification indices particularly for trade-offs between multiple traits. Lastly, we highlight the genetic mechanisms underpinning trade-offs and experimental designs that facilitate their discovery in plants, with focus on usage of natural variability. This review also offers a perspective for future research aimed at identification of plant trade-offs, dissection of their genetic architecture, and development of strategies to overcome trade-offs, with applications in crop breeding.
Processes governing genetic diversity and adaptive potential in reef-building corals are of interest both for fundamental evolutionary biology and for reef conservation. Here, we investigated the possibility of “sweepstakes reproductive success” (SRS) in a broadcast spawning coral Acropora hyacinthus at Yap Island, Micronesia. SRS is an extreme yearly variation in the number of surviving offspring among parents. It is predicted to generate genetically differentiated, low genetic diversity recruit cohorts, containing close kin individuals. We have tested these predictions by comparing genetic composition of size classes (adults and juveniles) at several sites on the island of Yap, Micronesia. We did see the genome-wide dip in genetic diversity in juveniles compared to adults at two of the four sites; however, both adults and juveniles varied in genetic diversity across sites, and there was no detectable genetic structure among juveniles, which does not conform to the classical SRS scenario. Yet, we have identified a pair of juvenile siblings at the site where juveniles had the lowest genetic diversity compared to adults, an observation that is hard to explain without invoking SRS. While further support for SRS is needed to fully settle the issue, we show that incorporating SRS into the Indo-West Pacific coral metapopulation adaptation model had surprisingly little effect on mean rates of coral cover decline during warming. Still, SRS notably increases year-to-year variation in coral cover throughout the simulation.
Distinguishing among the mechanisms underlying the spatial distribution of genetic variation resulting from the environmental or physical barriers from those arising due to simple geographic distance is challenging in complex landscapes. The Andean uplift represents one of the most heterogeneous habitats where these questions remain unexplored since multiple mechanisms may interact, confounding their relative roles. We explore this broad question in the leaf-cutting ant Atta cephalotes, a species that is distributed across the Andes mountains, using nuclear microsatellite markers and mtCOI gene sequences. We investigate spatial genetic divergence across the western range of the northern Andes in Colombia by testing the relative role of alternative scenarios of population divergence, including isolation by geographic distance (IBD), climatic conditions (IBE), and the physical barriers presented by the Andes mountains (IBB). Our results reveal substantial genetic differentiation among A. cephalotes populations for both types of markers, but only nuclear divergence followed a hierarchical pattern with multiple models of genetic divergence imposed by the western range. Model selection showed that the IBD, IBE (temperature and precipitation), and IBB (Andes mountains) models, often proposed as individual drivers of genetic divergence, interact and explain up to 33% of the genetic divergence in A. cephalotes. The IBE model remained significant after accounting for IBD, suggesting that environmental factors play a more prominent role than with IBB. These factors, in combination with the idiosyncratic dispersal patterns of ants, appear to determine the hierarchical patterns of gene flow. This study enriches our understanding of the forces shaping population divergence in complex habitat landscapes.
Many long-term genetic monitoring programs began before next-generation sequencing became widely available. Older programs can now transition to new marker systems usually consisting of 1000s of SNP loci, but there are still important questions about comparability, precision, and accuracy of key metrics estimated using SNPs. Ideally, transitioned programs should capitalize on new information without sacrificing continuity of inference across the time series. We combined existing microsatellite-based genetic monitoring information with SNP-based microhaplotypes obtained from archived samples of Rio Grande silvery minnow (Hybognathus amarus) across a 20-year time series to evaluate point estimates and trajectories of key genetic metrics. Demographic and genetic monitoring bracketed multiple collapses of the wild population, and included cases where captive-born repatriates comprised the majority of spawners in the wild. Even with smaller sample sizes, microhaplotypes yielded comparable and in some cases more precise estimates of variance genetic effective population size, multilocus heterozygosity and inbreeding compared to microsatellites because many more microhaplotype loci were available. Microhaplotypes also recorded shifts in allele frequencies associated with population bottlenecks. Trends in microhaplotype-based inbreeding metrics were associated with the fraction of hatchery-reared repatriates to the wild, and should be incorporated into future genomic monitoring. Although differences in accuracy and precision of some metrics were observed between marker types, biological inferences and management recommendations were consistent.
Speciation is a fundamental evolutionary process, which results in genetic differentiation of populations and manifests as discrete morphological, physiological and behavioral differences. Each species has had its own evolutionary trajectory, formed by many types of selection pressures and random drift, making the association of genetic differences between the species with the phenotypic differences extremely difficult. In the present study, we have used an in vitro model to analyze in depth the genetic and gene regulation differences between fibroblasts of two closely related mammals, the arctic/subarctic mountain hare (Lepus timidus Linnaeus) and the temperate steppe-climate adapted brown hare (Lepus europaeus Pallas). We discovered the existence of a species-specific expression pattern of 1,623 genes, manifesting in differences in cell growth, respiration, and metabolism. Interspecific differences in the housekeeping functions of fibroblast cells suggest speciation acts on fundamental processes, even in these two interfertile species. Our results help to understand the molecular constituents of a species difference on cellular level, which could contribute to the maintenance of the species boundary
The gut microbiota of bees affect nutrition, immunity, and host fitness, yet the role of diet, sociality, and geographic variation in determining microbiome structure, including strain-level diversity and relatedness, remain poorly understood. Here, we use full-length 16S amplicon sequencing to compare the crop and gut microbiomes of two incipiently social carpenter bee species, Xylocopa sonorina and Xylocopa tabaniformis, from multiple geographic sites within each species’ range. We found that Xylocopa species share a set of core taxa consisting of Bombilactobacillus, Bombiscardovia, and Lactobacillus apis, found in >95% of all individual bees sampled, and Gilliamella and Apibacter were also detected in the gut of both species with high frequency. The crop bacterial community of both species was comprised nearly entirely of Apilactobacillus with occasionally abundant nectar bacteria. Despite sharing core taxa, Xylocopa species’ microbiomes were distinguished by multiple bacterial lineages, including species-specific strains of core taxa. In both bee species, bacterial species exhibited geographic patterns in the presence of specific sequence variants. The use of long-read amplicons revealed otherwise cryptic species and population-level differentiation in core microbiome members which was masked when a shorter fragment of the 16S (V4) was considered. We conclude that these Xylocopa species host a distinctive microbiome, similar to that of previously characterized social apids, which suggests that further investigation to understand the evolution of bee microbiome and its drivers is warranted.
Studies of natural hybrid zones can provide documentation of range shifts in response to climate change and identify loci important to reproductive isolation. Using a deep temporal (36-38 years) comparison of the black-capped (Poecile atricapillus) and Carolina (P. carolinensis) chickadee hybrid zone, we investigated movement of the western portion of the zone (western Missouri) and assessed whether loci and pathways underpinning reproductive isolation were similar to those in the eastern portion of the hybrid zone. Using 92 birds sampled along the hybrid zone transect in 2016 and 68 birds sampled between 1978 and 1980, we generated 11,669 SNPs via ddRADseq. These SNPs were used to assess movement of the hybrid zone through time and to evaluate variation in introgression among loci. We demonstrate that the interface has moved ~5 km to the northwest over the last 36-38 years, i.e., at only one-fifth the rate at which the eastern portion (e.g., Pennsylvania, Ohio) of the hybrid zone has moved. Temperature trends over the last 38 years reveal that eastern areas have warmed 50% more than western areas in terms of annual mean temperature, possibly providing an explanation for the slower movement of the hybrid zone in Missouri. Our results suggest hybrid zone movement in broadly distributed species, such as chickadees, will vary between areas in response to local differences in the impacts of climate change.
Symbiosis often occurs between partners with distinct life history characteristics and dispersal mechanisms. Many bacterial symbionts have genomes comprised of multiple replicons with distinct rates of evolution and horizontal transmission. Such differences might drive differences in population structure between hosts and symbionts and among the elements of the divided genomes of bacterial symbionts. These differences might, in turn, shape the evolution of symbiotic interactions and bacterial evolution. Here we use whole genome resequencing of a hierarchically-structured sample of 191 strains of Sinorhizobium meliloti collected from 21 locations in southern Europe to characterize population structures of this bacterial symbiont and its host plant Medicago truncatula. Sinorhizobium meliloti genomes showed high local (within-site) variation and little isolation by distance. This was particularly true for the two symbiosis elements pSymA and pSymB, which have population structures that are similar to each other, but distinct from both the bacterial chromosome and the host plant. The differences in population structure may result from among-replicon differences in the extent of horizontal gene transfer, although given limited recombination of the chromosome, different levels of purifying or positive selection may also contribute to among-replicon differences. Discordant population structure between hosts and symbionts indicates that geographically and genetically distinct host populations in different parts of the range might interact with genetically similar symbionts, potentially minimizing local specialization.
Availability of suitable nectar and pollen resources is a limiting factor for pollinator survival, with both overall resource quantity and quality, along with provision throughout the season, being critical. Yet, our understanding of how the selection of floral resources changes over time, and how this relates to floral availability within the landscape is limited. To fill this knowledge gap, we characterise floral use by honeybee (Apis mellifera) colonies, in a diverse horticultural and agricultural landscape, from April to September, over two years, using pollen DNA metabarcoding of honey samples. We compared the pollen found to the availability of host plants within the surrounding landscape using floral surveys. Honeybees used a total of 143 plant taxa, but only 10 of these were determined as major sources (>10% of total sequence reads in any month) and total plant use represented a small proportion of the available floral resources (23% of genera). Distinct patterns of diet specialisation were identified in June and August, where colonies diverged in their floral preferences before re-aligning in July and September. Following optimal foraging theory, these patterns represent periods of resource limitation. Honeybees showed a preference for flowering trees in the spring, followed by shrubs and herbs in summer and used native and near-native plants more than horticultural plants, as major food sources. DNA metabarcoding allows an increased ecological insight into floral resource use by honeybees and highlights the importance of providing continuous and sufficient floral resources throughout the year.
Photosymbiodemes are a special case of lichen symbiosis where one lichenized fungus engages in symbiosis with two different photosynthetic partners, a cyanobacterium and a green alga, to develop two distinctly looking photomorphs. We investigated differential gene expression in photosymbiodemes of the lichen Peltigera britannica at different temperatures representing mild and putatively stressful conditions and compared gene expression of thallus sectors containing cyanobacterial photobionts with thallus sectors with both green algal and cyanobacterial photobionts. Firstly, because of known ecological differences between photomorphs, we investigated symbiont-specific responses in gene expression to temperature increases. Secondly, we quantified photobiont-mediated differences in fungal gene expression. High temperatures expectedly led to an upregulation of genes involved in heat shock responses in all organisms in whole transcriptome data. As expected, the expression of genes involved in photosynthesis was increased in both photobiont types at 15 and 25 °C. The green algae exhibited thermal stress responses mainly at 25 °C, the fungus and the cyanobacteria already at 15 °C, demonstrating symbiont-specific responses to environmental cues and symbiont-specific ecological optima. Furthermore, photobiont-mediated differences in fungal gene expression could be identified, with upregulation of distinct biological processes in the different morphs, showing that interaction with specific symbiosis partners profoundly impacts fungal gene expression.