Microevolutionary change in wild stickleback: Using integrative time-series data to infer responses to selection

Traits of wild animals can change over contemporary timescales, but concluding that evolution played a role requires demonstrating that trait change is linked to genetic change. This is because while selection acts on organisms? traits, evolution in the strict sense is a process resulting in changes to the genome. But natural selection operating in natural ecosystems rarely acts in a single direction, and many factors that cause selection vary through time. We study wild stickleback in a well-studied lake to characterize how the genetics of correlated traits respond to different types of selection (e.g., directional or fluctuating). Our study clearly demonstrates how evolutionary processes cause trait change in the wild on a contemporary timescale. A central goal in evolutionary biology is to understand how different evolutionary processes cause trait change in wild populations. However, quantifying evolutionary change in the wild requires linking trait change to shifts in allele frequencies at causal loci. Nevertheless, datasets that allow for such tests are extremely rare and existing theoretical approaches poorly account for the evolutionary dynamics that likely occur in ecological settings. Using a decade-long integrative phenome-to-genome time-series dataset on wild threespine stickleback (Gasterosteus aculeatus), we identified how different modes of selection (directional, episodic, and balancing) drive microevolutionary change in correlated traits over time. Most strikingly, we show that feeding traits changed by as much 25% across 10 generations which was driven by changes in the genetic architecture (i.e., in both genomic breeding values and allele frequencies at genetic loci for feeding traits). Importantly, allele frequencies at genetic loci related to feeding traits changed at a rate greater than expected under drift, suggesting that the observed change was a result of directional selection. Allele frequency dynamics of loci related to swimming traits appeared to be under fluctuating selection evident in periodic population crashes in this system. Our results show that microevolutionary change in a wild population is characterized by different modes of selection acting simultaneously on different traits, which likely has important consequences for the evolution of correlated traits. Our study provides one of the most thorough descriptions to date of how microevolutionary processes result in trait change in a natural population

Chironomidae fauna of springs in Iceland: Assessing the ecological relevance behind Tuxen’s spring classification

In 1937, S.L. Tuxen studied the animal community of hot springs in Iceland, and classified springs according to their relative temperature into cold, tepid, and hot. Eighty years after Tuxen’s study, we revisited some of the hot springs in Skagafjörður, Northern Iceland. Our aim was to compare the invertebrate community of 1937 and today, and to assess the stability of hot spring habitats over the years. To test Tuxen’s spring classification on an ecological basis, we furthermore collected chironomid larvae from 24 springs of a broad range of temperature, with samples taken both at the surface area of the spring and at the groundwater level. The chironomid species composition of hot springs differed from that of cold and tepid springs. Whereas Cricotopus sylvestris, Arctopelopia sp., and Procladius sp. characterised the chironomid community in Icelandic hot springs, cold and tepid springs were dominated by Eukiefferiella minor, Orthocladius frigidus and Diamesa spp. Community composition analyses and the exclusive occurrence of taxa in one of the temperature classes validated the ecological relevance of Tuxen’s spring classification for the chironomid species community. Both environmental parameters and invertebrate community of Icelandic hot springs seem to be the same as 80 years ago. Although springs have the potential to provide stable habitats, they are currently under high anthropogenic pressure, and should be increasingly considered in nature conservation.

Re-identification of individuals from images using spot constellations : a case study in Arctic charr (Salvelinus alpinus)

The long-term monitoring of Arctic charr in lava caves is funded by the Icelandic Research Fund, RANNÍS (research grant nos. 120227 and 162893). E.A.M. was supported by the Icelandic Research Fund, RANNÍS (grant no. 162893) and NERC research grant awarded to M.B.M. (grant no. NE/R011109/1). M.B.M. was supported by a University Research Fellowship from the Royal Society (London). C.A.L. and B.K.K. were supported by Hólar University, Iceland. The Titan Xp GPU used for this research was donated to K.T. by the NVIDIA Corporation.The ability to re-identify individuals is fundamental to the individual-based studies that are required to estimate many important ecological and evolutionary parameters in wild populations. Traditional methods of marking individuals and tracking them through time can be invasive and imperfect, which can affect these estimates and create uncertainties for population management. Here we present a photographic re-identification method that uses spot constellations in images to match specimens through time. Photographs of Arctic charr (Salvelinus alpinus) were used as a case study. Classical computer vision techniques were compared with new deep-learning techniques for masks and spot extraction. We found that a U-Net approach trained on a small set of human-annotated photographs performed substantially better than a baseline feature engineering approach. For matching the spot constellations, two algorithms were adapted, and, depending on whether a fully or semi-automated set-up is preferred, we show how either one or a combination of these algorithms can be implemented. Within our case study, our pipeline both successfully identified unmarked individuals from photographs alone and re-identified individuals that had lost tags, resulting in an approximately 4 our multi-step pipeline involves little human supervision and could be applied to many organisms.Publisher PDFPeer reviewe

Multigenerational exposure to elevated temperatures leads to a reduction in standard metabolic rate in the wild

In light of global climate change, there is a pressing need to understand and predict the capacity of populations to respond to rising temperatures. Metabolic rate is a key trait that is likely to influence the ability to cope with climate change. Yet, empirical and theoretical work on metabolic rate responses to temperature changes has so far produced mixed results and conflicting predictions. Our study addresses this issue using a novel approach of comparing fish populations in geothermally warmed lakes and adjacent ambient‐temperature lakes in Iceland. This unique ‘natural experiment' provides repeated and independent examples of populations experiencing contrasting thermal environments for many generations over a small geographic scale, thereby avoiding the confounding factors associated with latitudinal or elevational comparisons. Using Icelandic sticklebacks from three warm and three cold habitats, we measured individual metabolic rates across a range of acclimation temperatures to obtain reaction norms for each population. We found a general pattern for a lower standard metabolic rate in sticklebacks from warm habitats when measured at a common temperature, as predicted by Krogh's rule. Metabolic rate differences between warm‐ and cold‐habitat sticklebacks were more pronounced at more extreme acclimation temperatures, suggesting the release of cryptic genetic variation upon exposure to novel conditions, which can reveal hidden evolutionary potential. We also found a stronger divergence in metabolic rate between thermal habitats in allopatry than sympatry, indicating that gene flow may constrain physiological adaptation when dispersal between warm and cold habitats is possible. In sum, our study suggests that fish may diverge toward a lower standard metabolic rate in a warming world, but this might depend on connectivity and gene flow between different thermal habitats

Bacterial diversity in Icelandic cold spring sources and in relation to the groundwater amphipod Crangonyx islandicus

Publisher's version (útgefin grein)Crangonyx islandicus is a groundwater amphipod endemic to Iceland, considered to have survived the Ice Ages in subglacial refugia. Currently the species is found in spring sources in lava fields along the tectonic plate boundary of the country. The discovery of a groundwater species in this inaccessible habitat indicates a hidden ecosystem possibly based on chemoautotrophic microorganisms as primary producers. To explore this spring ecosystem, we assessed its microbial diversity and analysed whether and how the diversity varied between the amphipods and the spring water, and if was dependent on environmental factors and geological settings. Isolated DNA from spring water and from amphipods was analysed using metabarcoding methods, targeting the 16S rRNA gene. Two genera of bacteria, Halomonas and Shewanella were dominating in the amphipod samples in terms of relative abundance, but not in the groundwater samples where Flavobacterium, Pseudomonas and Alkanindiges among others were dominating. The richness of the bacteria taxa in the microbial community of the groundwater spring sources was shaped by pH level and the beta diversity was shaped by geographic locations.This work was supported by the Icelandic Research Council [grant number: 130244-051 to SP and 141863-051 to BKK] and by the doctoral fund at the University of Iceland. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Peer Reviewe

Patterns, processes, and conservation management consequences of intraspecific diversity, illustrated by fishes from recently glaciated lakes

Patterns in phenotypic and genotypic diversity within many species are becoming increasingly apparent, although there remain many species for which such patterns have yet to be described adequately. Fishes from recently glaciated ecosystems are likely to be particularly rich in intraspecific diversity, yet current conservation management strategies are, in many parts of the world, particularly in Europe, conventionally and overwhelmingly focused on species, regardless of competing species concepts, and appropriate policies for managing diversity at a sub-specific level still have to be developed. Occasional attempts to protect certain vulnerable ecotypes and proposed alternative units of conservation (e.g. ‘Pragmatic Species’ or ‘Evolutionarily Significant Units’) reinforce the conventional primacy of contemporary expressed patterns of variation. Intraspecific phenotypic and genotypic patterns are ultimately the result of complex processes of divergence; conservation approaches that focus on the products of evolution largely ignore the processes that generate and maintain those patterns. Policies that acknowledge the continuation of evolution, the derivation of novel diversity over often very short time spans and the role of environment in initiating and perpetuating these processes are poorly integrated into management strategy. To address possible deficits, where intraspecific diversity is not addressed in management practice, we believe it to be important first to characterize hidden genetic and phenotypic diversity, which may intimate eco-evolutionary processes, initially among species of high conservation status. A second step should be to use an approach to intraspecific diversity that illuminates the ultimate processes and mechanisms that bring about that diversity, which also concedes the central role of the environment and affords adequate protection to the ecosystems that drive these processes, such as the United Nations Convention on Biological Diversity (CBD) Ecosystems approach

What is a fish? The life and legend of David L.G. Noakes

David Lloyd George Noakes (1942–2020) is best known for his insatiable curiosity, his quick wit and dry sense of humor, his scientific contributions to the field of animal behaviour, and his ability to form and maintain long-lasting connections. His research interests were vast but remained grounded in early life history, behaviour, social behaviour, the evolution of behaviour, behavioural genetics, and evolutionary ecology. David had a remarkable ability to establish and maintain strong connections within the international academic community. David was also internationally recognized for his numerous contributions as a scientific editor, promoting accessibility to the international community that he served. We memorialize David’s legacy in this tribute article, ensuring that his accomplishments and the momentous impact he had on the scientific community are not soon forgotten

Gene expression in the phenotypically plastic Arctic charr (Salvelinus alpinus): A focus on growth and ossification at early stages of development

Publisher's version (útgefin grein)Gene expression during development shapes the phenotypes of individuals. Although embryonic gene expression can have lasting effects on developmental trajectories, few studies consider the role of maternal effects, such as egg size, on gene expression. Using qPCR, we characterize relative expression of 14 growth and/or skeletal promoting genes across embryonic development in Arctic charr (Salvelinus alpinus). We test to what extent their relative expression is correlated with egg size and size at early life‐stages within the study population. We predict smaller individuals to have higher expression of growth and skeletal promoting genes, due to less maternal resources (i.e., yolk) and prioritization of energy toward ossification. We found expression levels to vary across developmental stages and only three genes (Mmp9, Star, and Sgk1) correlated with individual size at a given developmental stage. Contrary to our hypothesis, expression of Mmp9 and Star showed a non‐linear relationship with size (at post fertilization and hatching, respectively), whilst Sgk1 was higher in larger embryos at hatching. Interestingly, these genes are also associated with craniofacial divergence of Arctic charr morphs. Our results indicate that early life‐stage variation in gene expression, concomitant to maternal effects, can influence developmental plasticity and potentially the evolution of resource polymorphism in fishes.We thank John Postlethwait for his valuable comments on the manuscript. This research was funded by the Icelandic Research Fund, Rannis (grant number 141360 to CAL et al., and grant number 173814–051 to SVB).Peer Reviewe

Geothermal stickleback populations prefer cool water despite multigenerational exposure to a warm environment

Given the threat of climate change to biodiversity, a growing number of studies are investigating the potential for organisms to adapt to rising temperatures. Earlier work has predicted that physiological adaptation to climate change will be accompanied by a shift in temperature preferences, but empirical evidence for this is lacking. Here, we test whether exposure to different thermal environments has led to changes in preferred temperatures in the wild. Our study takes advantage of a “natural experiment” in Iceland, where freshwater populations of threespine sticklebacks (Gasterosteus aculeatus) are found in waters warmed by geothermal activity year-round (warm habitats), adjacent to populations in ambient-temperature lakes (cold habitats). We used a shuttle-box approach to measure temperature preferences of wild-caught sticklebacks from three warm–cold population pairs. Our prediction was that fish from warm habitats would prefer higher water temperatures than those from cold habitats. We found no support for this, as fish from both warm and cold habitats had an average preferred temperature of 13°C. Thus, our results challenge the assumption that there will be a shift in ectotherm temperature preferences in response to climate change. In addition, since warm-habitat fish can persist at relatively high temperatures despite a lower-temperature preference, we suggest that preferred temperature alone may be a poor indicator of a population's adaptive potential to a novel thermal environment

Seasonal variation in the invertebrate community and diet of a top fish predator in a thermally stable spring

Many life-history events in aquatic invertebrates are triggered by seasonal changes in water temperature, but other ecological factors may be important as well. To rule out the confounding effects of changing water temperature, we studied the seasonal dynamics of an aquatic invertebrate community and their effect on a top fish predator in a thermally stable freshwater spring in South Iceland. We sampled benthic invertebrates five times over a year and conducted a mark-recapture study on the top predator in the system, small benthic Arctic charr, Salvelinus alpinus (L.). We assessed variation in diet composition and feeding preferences by calculating the electivity and individual specialisation of each fish at each sampling time. There was a clear separation of winter and summer communities for the benthic invertebrates. The variation in prey availability was also reflected in the fish diet, with higher feeding selectivity in summer than in winter for the highly abundant Chironomidae larvae. In contrast, individual specialisation as a measure of intrapopulation niche variation was higher in winter when prey availability was lower. We furthermore found that groundwater amphipods might play an important role in the winter diet of spring-dwelling Arctic charr. In conclusion, seasonal variation in the invertebrate community is an important factor to consider and has the potential to alter the phenotype (e.g. growth rates) and behaviour (e.g. feeding preferences) of higher trophic levels