Disentangling the drivers of decadal body size decline in an insect population.

While climate warming is widely predicted to reduce body size of ectotherms, evidence for this trend is mixed. Body size depends not only on temperature but also on other factors, such as food quality and intraspecific competition. Because temperature trends or other long-term environmental factors may affect population size and food sources, attributing trends in average body size to temperature requires the separation of potentially confounding effects. We evaluated trends in the body size of the midge Tanytarsus gracilentus and potential drivers (water temperature, population size, and food quality) between 1977 and 2015 at Lake Mývatn, Iceland. Although temperatures increased at Mývatn over this period, there was only a slight (non-significant) decrease in midge adult body size, contrary to theoretical expectations. Using a state-space model including multiple predictors, body size was negatively associated with both water temperature and midge population abundance, and it was positively associated with 13 C enrichment of midges (an indicator of favorable food conditions). The magnitude of these effects were similar, such that simultaneous changes in temperature, abundance, and carbon stable isotopic signature could counteract each other in the long-term body size trend. Our results illustrate how multiple factors, all of which could be influenced by global change, interact to affect average ectotherm body size.

Demographic Basis of Spatially Structured Fluctuations in a Threespine Stickleback Metapopulation.

AbstractUncovering the demographic basis of population fluctuations is a central goal of population biology. This is particularly challenging for spatially structured populations, which require disentangling synchrony in demographic rates from coupling via movement between locations. In this study, we fit a stage-structured metapopulation model to a 29-year time series of threespine stickleback abundance in the heterogeneous and productive Lake Mývatn, Iceland. The lake comprises two basins (North and South) connected by a channel through which the stickleback disperse. The model includes time-varying demographic rates, allowing us to assess the potential contributions of recruitment and survival, spatial coupling via movement, and demographic transience to the population's large fluctuations in abundance. Our analyses indicate that recruitment was only modestly synchronized between the two basins, whereas survival probabilities of adults were more strongly synchronized, contributing to cyclic fluctuations in the lake-wide population size with a period of approximately 6 years. The analyses further show that the two basins were coupled through movement, with the North Basin subsidizing the South Basin and playing a dominant role in driving the lake-wide dynamics. Our results show that cyclic fluctuations of a metapopulation can be explained in terms of the combined effects of synchronized demographic rates and spatial coupling.

Genome-phenotype-environment associations identify signatures of selection in a panmictic population of threespine stickleback.

Adaptive genetic divergence occurs when selection imposed by the environment causes the genomic component of the phenotype to differentiate. However, genomic signatures of natural selection are usually identified without information on which trait is responding to selection by which selective agent(s). Here, we integrate whole-genome sequencing with phenomics and measures of putative selective agents to assess the extent of adaptive divergence in threespine stickleback occupying the highly heterogeneous lake Mývatn, NE Iceland. We find negligible genome wide divergence, yet multiple traits (body size, gill raker structure and defence traits) were divergent along known ecological gradients (temperature, predatory bird densities and water depth). SNP based heritability of all measured traits was high (h2  = 0.42-0.65), indicating adaptive potential for all traits. Environment-association analyses further identified thousands of loci putatively involved in selection, related to genes linked to, for instance, neuron development and protein phosphorylation. Finally, we found that loci linked to water depth were concurrently associated with pelvic spine length variation - supporting the conclusion that divergence in pelvic spine length occurred in the face of gene flow. Our results suggest that whilst there is substantial genetic variation in the traits measured, phenotypic divergence of Mývatn stickleback is mostly weakly associated with environmental gradients, potentially as a result of substantial gene flow. Our study illustrates the value of integrative studies that combine genomic assays of multivariate trait variation with landscape genomics.

Positive feedback between chironomids and algae creates net mutualism between benthic primary consumers and producers.

The chironomids of Lake Mývatn show extreme population fluctuations that affect most aspects of the lake ecosystem. During periods of high chironomid densities, chironomid larvae comprise over 90% of aquatic secondary production. Here, we show that chironomid larvae substantially stimulate benthic gross primary production (GPP) and net primary production (NPP), despite consuming benthic algae. Benthic GPP in experimental mesocosms with 140,000 larvae/m2 was 71% higher than in mesocosms with no larvae. Similarly, chlorophyll a concentrations in mesocosms increased significantly over the range of larval densities. Furthermore, larvae showed increased growth rates at higher densities, possibly due to greater benthic algal availability in these treatments. We investigated the hypothesis that larvae promote benthic algal growth by alleviating nutrient limitation, and found that (1) larvae have the potential to cycle the entire yearly external loadings of nitrogen and phosphorus during the growing season, and (2) chlorophyll a concentrations were significantly greater in close proximity to larvae (on larval tubes). The positive feedback between chironomid larvae and benthic algae generated a net mutualism between the primary consumer and primary producer trophic levels in the benthic ecosystem. Thus, our results give an example in which unexpected positive feedbacks can lead to both high primary and high secondary production.

Identifying consumer-resource population dynamics using paleoecological data.

Ecologists have long been fascinated by cyclic population fluctuations, because they suggest strong interactions between exploiter and victim species. Nonetheless, even for populations showing high-amplitude fluctuations, it is often hard to identify which species are the key drivers of the dynamics, because data are generally only available for a single species. Here, we use a paleoecological approach to investigate fluctuations in the midge population in Lake Mývatn, Iceland, which ranges over several orders of magnitude in irregular, multigeneration cycles. Previous circumstantial evidence points to consumer-resource interactions between midges and their primary food, diatoms, as the cause of these high-amplitude fluctuations. Using a pair of sediment cores from the lake, we reconstructed 26 years of dynamics of midges using egg remains and of algal groups using diagnostic pigments. We analyzed these data using statistical methods that account for both the autocorrelated nature of paleoecological data and measurement error caused by the mixing of sediment layers. The analyses revealed a signature of consumer-resource interactions in the fluctuations of midges and diatoms: diatom abundance (as inferred from biomarker pigment diatoxanthin) increased when midge abundance was low, and midge abundance (inferred from egg capsules) decreased when diatom abundance was low. Similar patterns were not found for pigments characterizing the other dominant primary producer group in the lake (cyanobacteria), subdominant algae (cryptophytes), or ubiquitous but chemically unstable biomarkers of total algal abundance (chlorophyll a); however, a significant but weaker pattern was found for the chemically stable indicator of total algal populations (ß-carotene) to which diatoms are the dominant contributor. These analyses provide the first paleoecological evaluation of specific trophic interactions underlying high amplitude population fluctuations in lakes.

High-amplitude fluctuations and alternative dynamical states of midges in Lake Myvatn.

Complex dynamics are often shown by simple ecological models and have been clearly demonstrated in laboratory and natural systems. Yet many classes of theoretically possible dynamics are still poorly documented in nature. Here we study long-term time-series data of a midge, Tanytarsus gracilentus (Diptera: Chironomidae), in Lake Myvatn, Iceland. The midge undergoes density fluctuations of almost six orders of magnitude. Rather than regular cycles, however, these fluctuations have irregular periods of 4-7 years, indicating complex dynamics. We fit three consumer-resource models capable of qualitatively distinct dynamics to the data. Of these, the best-fitting model shows alternative dynamical states in the absence of environmental variability; depending on the initial midge densities, the model shows either fluctuations around a fixed point or high-amplitude cycles. This explains the observed complex population dynamics: high-amplitude but irregular fluctuations occur because stochastic variability causes the dynamics to switch between domains of attraction to the alternative states. In the model, the amplitude of fluctuations depends strongly on minute resource subsidies into the midge habitat. These resource subsidies may be sensitive to human-caused changes in the hydrology of the lake, with human impacts such as dredging leading to higher-amplitude fluctuations. Tanytarsus gracilentus is a key component of the Myvatn ecosystem, representing two-thirds of the secondary productivity of the lake and providing vital food resources to fish and to breeding bird populations. Therefore the high-amplitude, irregular fluctuations in midge densities generated by alternative dynamical states dominate much of the ecology of the lake.

Shared Features Underlying Compact Genomes and Extreme Habitat Use in Chironomid Midges.

Nonbiting midges (family Chironomidae) are found throughout the world in a diverse array of aquatic and terrestrial habitats, can often tolerate harsh conditions such as hypoxia or desiccation, and have consistently compact genomes. Yet we know little about the shared molecular basis for these attributes and how they have evolved across the family. Here, we address these questions by first creating high-quality, annotated reference assemblies for Tanytarsus gracilentus (subfamily Chironominae, tribe Tanytarsini) and Parochlus steinenii (subfamily Podonominae). Using these and other publicly available assemblies, we created a time-calibrated phylogenomic tree for family Chironomidae with outgroups from order Diptera. We used this phylogeny to test for features associated with compact genomes, as well as examining patterns of gene family evolution and positive selection that may underlie chironomid habitat tolerances. Our results suggest that compact genomes evolved in the common ancestor of Chironomidae and Ceratopogonidae and that this occurred mainly through reductions in noncoding regions (introns, intergenic sequences, and repeat elements). Significantly expanded gene families in Chironomidae included biological processes that may relate to tolerance of stressful environments, such as temperature homeostasis, carbohydrate transport, melanization defense response, and trehalose transport. We identified several positively selected genes in Chironomidae, notably sulfonylurea receptor, CREB-binding protein, and protein kinase D. Our results improve our understanding of the evolution of small genomes and extreme habitat use in this widely distributed group.

Reconstructing midge consumer-resource dynamics using carbon stable isotope signatures of archived specimens.

Population cycles can be caused by consumer-resource interactions. Confirming the role of consumer-resource interactions, however, can be challenging due to an absence of data for the resource candidate. For example, interactions between midge larvae and benthic algae likely govern the high-amplitude population fluctuations of Tanytarsus gracilentus in Lake Mývatn, Iceland, but there are no records of benthic resources concurrent with adult midge population counts. Here, we investigate consumer population dynamics using the carbon stable isotope signatures of archived T. gracilentus specimens collected from 1977 to 2015, under the assumption that midge δ13 C values reflect those of resources they consumed as larvae. We used the time series for population abundance and δ13 C to estimate interactions between midges and resources while accounting for measurement error and possible preservation effects on isotope values. Results were consistent with consumer-resource interactions: high δ13 C values preceded peaks in the midge population, and δ13 C values tended to decline after midges reached high abundance. One interpretation of this dynamic coupling is that midge isotope signatures reflect temporal variation in benthic algal δ13 C values, which we expected to mirror primary production. Following from this explanation, high benthic production (enriched δ13 C values) would contribute to increased midge abundance, and high midge abundance would result in declining benthic production (depleted δ13 C values). An additional and related explanation is that midges deplete benthic algal abundance once they reach peak densities, causing midges to increase their relative reliance on other resources including detritus and associated microorganisms. Such a shift in resource use would be consistent with the subsequent decline in midge δ13 C values. Our study adds evidence that midge-resource interactions drive T. gracilentus fluctuations and demonstrates a novel application of stable isotope time-series data to understand consumer population dynamics.

Spatial phenotypic and genetic structure of threespine stickleback (Gasterosteus aculeatus) in a heterogeneous natural system, Lake Mývatn, Iceland.

Eco-evolutionary responses of natural populations to spatial environmental variation strongly depend on the relative strength of environmental differences/natural selection and dispersal/gene flow. In absence of geographic barriers, as often is the case in lake ecosystems, gene flow is expected to constrain adaptive divergence between environments - favoring phenotypic plasticity or high trait variability. However, if divergent natural selection is sufficiently strong, adaptive divergence can occur in face of gene flow. The extent of divergence is most often studied between two contrasting environments, whereas potential for multimodal divergence is little explored. We investigated phenotypic (body size, defensive structures, and feeding morphology) and genetic (microsatellites) structure in threespine stickleback (Gasterosteus aculeatus) across five habitat types and two basins (North and South) within the geologically young and highly heterogeneous Lake Mývatn, North East Iceland. We found that (1) North basin stickleback were, on average, larger and had relatively longer spines than South basin stickleback, whereas (2) feeding morphology (gill raker number and gill raker gap width) differed among three of five habitat types, and (3) there was only subtle genetic differentiation across the lake. Overall, our results indicate predator and prey mediated phenotypic divergence across multiple habitats in the lake, in face of gene flow.