Dipartimento di Scienze Ecologiche e Biologiche
A hotspot on fire: predicted impact of climate change on genetic diversity and disease tolerance in the endangered Apennine yellow-bellied toad Bombina pachypus
Author(s): Zampiglia, M, Canestrelli, D, Bisconti, R, Chiocchio, A, Nascetti, G
Climate change, emerging infectious diseases and levels of population genetic diversity can ‘conspire’ in yielding the decline and extinction of populations and species. We modeled species distribution and carried out a climate change vulnerability assessment for the endangered Bombina pachypus, an Italian endemic toad recently hypothesized to be faced with such ‘conspiracy’. For this species, southern Italy is the hotspot of genetic diversity and of disease tolerance to the chytrid pathogen Batrachochytrium dendrobatidis. This area showed the highest bioclimatic suitability for B. pachypus based on data for the years 1951-2000. Forecasted species distribution to 2080, under various models and emission scenarios, suggests that this area will become progressively less suitable, or even unsuitable for B. pachypus. Thus, loosing most of its evolutionary potential and historical resources to cope with chytrid outbreaks, B. pachypus will face a high extinction risk in the near future. On the other hand, in the northern regions, where populations are almost genetically invariable and demographically inconsistent, habitat suitability is predicted to increase in the near future. We suggest that captive breeding programs aimed at supporting translocation of genetic diversity from southern into northern populations (i.e. genetic rescue), are the only conservation actions with non-null probability to counteract this negative trend, and to attempt avoiding the human-driven extinction of this threatened amphibian species.
Department of Aquatic Ecology
Adaptive potential in a snail population
Author(s): Leicht, K, Seppälä, O
Adaptation to climate conditions is crucial for the existence and distribution of species and knowledge of adaptive potential will help us to predict how populations will be affected by climate change. Within-population genetic variation is the prior requirement for adaptation to changing environmental conditions, e.g. global warming. Here we examined if genetic variation in the responses to environmental change exists in a freshwater snail Lymnaea stagnalis. We exposed maternal family-lines originating from a Swiss snail population to thermal conditions similar to those during heat waves and assessed its effect on snail reproduction and immunocompetence. We found that high temperature increased snail reproduction and reduced immunocompetence. In addition we found family-level variation in snail reproduction and in all measured immune traits. However, we did not find family-level variation in response to a rise in temperature in any trait we measured indicated by non-significant family by temperature interactions. This suggests limited genetic potential to adapt to the predicted increase in the frequency of heat waves owing to climate change.
Department of Biology
Characterization of expression quantitative trait loci (eQTL) associated with response to thermal stress in the threespine stickleback, Gasterosteus aculeatus
Author(s): Pritchard, VL, Merilä, J, Nikinmaa, M, Primmer, C, Sävilammi, T, Viitaniemi, H, Leder, E
Ongoing climate change will expose populations to altered thermal regimens, which are likely to include more frequent and higher temperature maxima. Whether and how a resident population can withstand or adapt to these new conditions will depend on the genetic architecture underlying responses to temperature changes. This includes both coding genes and the regulatory regions that govern expression of these genes. Recent advances enabling the quantification of transcription levels for a large number of genes and the genotyping of many thousands of genetic markers throughout the genome, together with novel statistical methods, are facilitating the identification of such regulatory regions via expression quantitative trait locus (eQTL) analysis.
The threespine stickleback (Gasterosteus aculeatus) is an important model organism in evolutionary biology. The species occurs as resident populations in a wide range of habitats with different thermal profiles. We used sticklebacks derived from the Baltic coast of Finland to identify and localize eQTLs underlying changes in gene expression in response to thermal stress. Experimental subjects comprised 600 individuals in 30 sib–halfsib families, half of which were subject to a thermal challenge immediately prior to tissue collection. Liver mRNA expression was subsequently quantified using Agilent custom microarrays. Over 2000 genes were found to be differentially expressed between control and treatment groups. Genotyping of the families by sequencing on the Illumina platform, in combination with the existing G. aculeatus genome, was used to generate a linkage map that included over 10,000 SNPs. This enabled us to characterize and explore the regulatory networks underlying these changes in gene expression.
Department of Biological and Environmental Sciences
Climate and trematode-mollusk relationship
Author(s): Taskinen, J, Choo, JM
In trematode-mollusk relationships, climate warming may affect cercaria larvae production, virulence and competition between parasite species. In the present study we investigated the host-parasite relationship of the bucephalid trematodes Rhipidocotyle fennica and R. campanula which are transmitted from the unionid bivalve A. anatina to the second host, cyprinid fish Rutilus rutilus, via cercariae produced in the bivalve host. Results suggest that the annual period of cercarial production has become markedly longer in both parasite species from 1980’s to 2012—during the period of a climatic increase in temperature and length of summer. As compared to R. fennica, the parasite R. campanula started to produce cercariae much earlier in summer, resulting in a longer ceracariae production period annually. Early start of larval production was made possible in R. campanula by having cercaria production machinery ‘on standby’ throughout the year while R. fennica become inactive during winter. In line with this, R. campanula occurred in higher prevalences than R. fennica in northern areas, opposite to the south. The shorter summers towards north eventually limit the cercariae production period of the parasites, but due to the earlier onset of cercarial emission R. campanula is probably able to inhabit higher latitudes than R. fennica. However, R. campanula appeared to be more virulent than R. fennica (in terms of host survival and reproduction) which may be a cost of R. campanula’s ability to start cercariae production early seasonally. Impact of experimental temperature increase on annual cercarial production was positive in R. fennica but zero or negative in R. campanula. Thus, climate warming should benefit more R. fennica, and expand its range to the north. To conclude, climate change will presumably affect geographic distribution and abundance of Rhipidocotyle parasites, as well as modify the evolution of their virulence.
Climate change, host-parasite interactions and species invasions: an experiment initiated by Nature
Author(s): Wendling, CC, Wegner, MK
Biological invasions can be considered as an experiment performed by nature. They offer a unique way to study adaptation to new environments with all facets of new biotic and abiotic challenges like climate change and disease. On top of that, rising temperatures and risk of disease can interact and intensify selection pressure on invasive species to immunologically adapt to local parasites. The invasion of the Pacific oyster, Crassostrea gigas into the North Sea, is an ideal system to study the interactive effects of climate change and disease. Two independent invasions lead to the establishment of two genetically distinct populations, that differ in their selective history of disease outbreaks. While the Southern population is frequently subjected to natural selection induced by oyster summer mortality, with mortality rates exceeding 60%, Northern populations and hybrids in a secondary contact zone have been spared so far. Here, the interaction of high temperatures and bacteria of the genus Vibrio are believed to be the main causative agents of such mortalities. To test for differential selection gradients within the two invasion waves, we infected wild and artificially bred oysters with allopatric and sympatric Vibrio splendidus strains at prevailing and proposed future water temperatures. Based on mortality rates, immune response, and bacterial infection loads we observed that at high water temperatures oysters were severely impacted by Vibrio infection. However, while we consistently observed specific host immunological adaptation to sympatric parasites also at lower temperatures, direct advantages in terms of host fitness could only be detected at high temperatures indicating that the selective environment can unveil otherwise cryptic patterns of local adaptation.
Institute of Hydrobiology
Climate warming: Who suffers more in a host-parasite
Author(s): Dusi, E, Krenek, S, Sachse, R, Kaltz, O, Berendonk, TU
Climate change can alter species distributions, interactions and community compositions. Further, it can accelerate evolutionary processes. In host-parasite interactions it is difficult to predict whether the parasite or the host benefits most from global warming, because milder winter periods or higher nighttime temperatures can cause changes in development or transmission rates and may support the host/parasite. This study focuses on parasite virulence and prevalence in the context of stressful temperature conditions. We examined different strains of the host species Paramecium tetraurelia, a common freshwater ciliate, infected with the obligate intracellular bacterium Caedibacter taeniospiralis. This parasite is located in the cytoplasm of its host and vertically transmitted. An experimental approach was used to investigate if parasite virulence, defined as host’s fitness reduction caused by the parasite, is increasing under acute stress temperature conditions. Fitness of infected and uninfected P. tetraurelia was measured and the fitness-reduction/virulence was calculated at five different temperatures including a host stress temperature. The virulence caused by C. taeniospiralis was rising with higher temperature, but parasite prevalence was reduced at the host stress temperature. In an evolutionary context, the parasite could go extinct under acute stress conditions and the host would become cured of infection. Therefore, it was also tested how the parasite evolves under stress and optimum temperatures in long-term. The parasites that evolved under stress conditions seem to reduce costs to the host while having a higher prevalence compared to parasites that evolved under optimal conditions. Acute and intense stress might harm the parasite and seem to cause its extinction, but the parasite appears to be able to evolve and adapt to high-temperature stress conditions as caused by climate change.
Department of Biology & Environment
Co-evolution overrides climate change in cuckoo and reed warbler arms-race
Author(s): Markman, S, Berkowic, D, Stokke, BG, Meiri, S
The evolution of host organisms is influenced by their parasites and vice versa, and a co-evolutionary arms race often develops between the two. Evolution is also influenced by climate, but the interaction between co-evolution and climate has largely been overlooked. Here, we show that the co-evolutionary arms race between the parasitic common cuckoo (Cuculus canorus) and its host, the reed warbler (Acrocephalus scirpaceus), overrides climatic factors in affecting the egg sizes of both species. Cuckoo egg volume decreased during the 20th century while reed warbler egg volume in parasitized nests increased, resulting in cuckoo eggs that were closer in size to those of the reed warbler. Egg volumes of sympatric reed warblers in non-parasitized nests, however, remained stable during that period. Cuckoo body size indices remained constant or increased over the same period, whereas reed warbler body size remained stable. Temperature and precipitation were uncorrelated with egg volume of either species. We suggest that cuckoos evolved to lay smaller eggs, to reduce rejection probability. Furthermore, our results point to the possibility that cuckoos may actively selected host nests with the largest host eggs. We suggest that cuckoos recently gained the upper hand in their co-evolutionary arms race with reed warblers, overriding the effects of recent climatic changes.
Institute of Environmental Sciences
Complex response in life history traits of the bulb mites in elevated thermal conditions – an experimental evolution approach
Author(s): Plesnar-Bielak, A, Jawor, A, Kramarz, P
Temperature is a key environmental factor affecting almost all the aspects of life histories in ectotherms. The theory predicts that organisms grow faster, reach smaller sizes and produce smaller offspring when temperature increases. In addition, temperature changes, through their effects on metabolism, may also influence the expression of alternative reproductive phenotypes (ARP). Although many studies investigated reaction norms of life history traits in relation to temperature change, little is known about how these reaction norms evolve. In our study we subjected the bulb mites to experimental evolution in two temperature treatments: control and elevated. After 18 generations we measured adult body size, eggs size and development time of both treatments at control as well as at elevated temperature. Thus, we were able to distinguish genetic changes (the effect of selection temperature) from environmental effects. The ARP expression was recorded in each generation. We found that mites developed faster and reached smaller sizes at increased temperature, but genetic effects of thermal adaptation were not always parallel to the observed reaction norms revealing quite complex patterns of life history traits response to temperature. Despite smaller body sizes females laid larger eggs at higher temperature. This effect was more pronounced in animals evolving at elevated temperature. Evolution at increased temperature affected also ARP expression with the proportion of armored fighters decreasing from generation to generation. We propose that this could be the consequence of temperature sensitiveness of cost to benefits ratio of expressing ARPs.
Department of Biology - Genetics
Constrating signatures of thermal stability evolution in ray-finned fish mitochondrial DNA-encoded proteins
Author(s): Bruneaux, M, Thalmann, O, Vasemägi, A, Primmer, C
Ray-finned fishes (actinopterygii) have successfully colonized almost all aquatic habitats, exploiting a wide range of temperature, salinity, oxygen level and hydrostatic pressure conditions. Temperature in particular is a strong environmental constraint driving adaptation, and several recent studies have detected signals of selection on mitochondrial genome along latitudinal or altitudinal gradients as well as an interaction between mitochondrial and nuclear genotypes in determining metabolic performance. Numerous actinopterygii complete mitochondrial genomes are now available and crystallographic structures have been determined for most of the 13 mitochondrial DNA-encoded proteins. Concomitantly, studies of the structural differences between mesophilic and thermophilic (optimal growth temperature > 50°C) microorganisms have provided useful insights into the general evolutionary patterns leading to increased protein thermal stability. In this context, we used all currently available actinopterygii mitochondrial genomes in relation with an environmental database (FishBase) to test whether there was an association between the thermal stability of mtDNA-encoded proteins and the environmental temperature commonly inhabited by the species. Several predictors of thermal stability (local structural entropy, amino acid compositional bias, hydrophobicity) were used with and without prior partitioning of the protein sequences into transmembrane and exposed regions. Phylogenetically independent contrasts were calculated to test the relationship between stability and environmental temperature. Signatures of increased predicted thermal stability with increasing environmental temperature were detected for some but not all of the proteins, thus suggesting that environmental temperature constrains the evolution of mtDNA-encoded protein stability in ray-finned fishes but that this constraint is not homogeneous among proteins.
Vector-borne Viral Diseases programme
Ecological niche evolution, phylogeography and thermal adaptation studies in Drosophila americana suggest it is a plastic species
Author(s): Morales-Hojas, R, Sillero, N, Reis, M, Vieira, C, Vieira, J
The study of ecological niche evolution is fundamental to understand how the environment influences species distributions and the role it plays in adaptation to divergent environments and species formation. Drosophila americana is widely distributed in North America. It comprises two chromosomal forms distributed in a north-south cline (chromosomes X/4 fused and non-fused, respectively), which is maintained by selection. Here we present a study of the ecological niche evolution and thermal adaptation of D. americana and the two chromosomal forms with the aim of understanding how they respond to a variety of environmental conditions. For this, we have used Ecological Niche Modelling, phylogeographic analysis and performance (locomotor and developmental time) experiments. Temperature is the environmental factor that contributes most to the ecological niches, although the relevance of precipitation is also high in the model of the Southern populations. Thermal performance experiments show no difference in the locomotor activity across a temperature range of 15º to 38ºC between flies from the north and the south of its distribution. Finally, we have modelled the past distribution of the species; its range during the last glacial maximum (LGM) was reduced to the southernmost of North America, while they had a similar distribution during the last interglacial (LIG) as currently. Analysis of the demographic history, nevertheless, detects no bottlenecks during the LGM. These results suggest that D. americana displays a plastic adaptation to the different temperatures of their distribution and do not support niche conservatism in Drosophila.