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Ellers, J.

Publications and source records attributed to Ellers, J..

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Additive effects of environmental and demographic variation shape the repeatability of evolution across replicated experiments

The repeatability of evolution is fundamentally important for understanding the origin and diversification of life as well as for developing evolutionary forecasting tools. Repeatability is limited by stochasticity, here defined as changes that are independent of genotypic fitness effects. Over short timescales, the two main sources of stochasticity of evolutionary change are environmental stochasticity and demographic (life-history) stochasticity. Quantifying the relative importance of these two sources of stochasticity in driving fitness outcomes is crucially important for predicting evolutionary responses. To gain insights in the effects of stochasticity, five institutes replicated an evolutionary experiment exposing Caenorhabditis elegans to novel rearing conditions. Replication across the institutes led to variation in selective environments, e.g. through divergent microbiomes among institutes. Replication within institutes was done across demographic treatments that influence the potential for population-size dependent fluctuations in allele frequencies (drift) and genetic hitchhiking (draft). We found high among-institute variation in fitness outcomes, which was partially explained by variation in microbiota. Whereas lab-specific effects explained most of the variance in mean fitness, the repeatability of fitness outcomes depended more on demographic heterogeneity. Specifically, population bottlenecks resulted in high among-replicate variation in fitness. When combined, environmental and demographic stochasticity additively reduced repeatability, underlining their additive importance in developing evolutionary forecasting tools. These results further highlight the importance of statistically integrating heterogeneity in experimental evolution to identify factors constraining outcome repeatability and study replicability.

evolutionary biology↗

Predicting the functional impact of single nucleotide variants in Drosophila melanogaster with FlyCADD

Understanding how genetic variants drive phenotypic differences is a major challenge in molecular biology. Single nucleotide polymorphisms form the vast majority of genetic variation and play critical roles in complex, polygenic phenotypes, yet their functional impact is poorly understood from traditional gene-level analyses. In-depth knowledge about the impact of single nucleotide polymorphisms has broad applications in health and disease, population genomic and evolution studies. The wealth of genomic data and available functional genetic tools make Drosophila melanogaster an ideal model species for studies at single nucleotide resolution. However, to leverage these resources for genotype-phenotype research and potentially combine it with the power of functional genetics, it is essential to develop techniques to predict functional impact and causality of single nucleotide variants. Here, we present FlyCADD, a functional impact prediction tool for single nucleotide variants in D. melanogaster. FlyCADD, based on the Combined Annotation-Dependent Depletion (CADD) framework, integrates over 650 genomic features - including conservation scores, GC content, and DNA secondary structure - into a single metric reflecting a variants predicted impact on evolutionary fitness. FlyCADD provides impact prediction scores for any single nucleotide variant on the D. melanogaster genome. We demonstrate the power of FlyCADD for typical applications, such as the ranking of phenotype-associated variants to prioritize variants for follow-up studies, evaluation of naturally occurring polymorphisms, and refining of CRISPR-Cas9 experimental design. FlyCADD provides a powerful framework for interpreting the functional impact of any single nucleotide variant in D. melanogaster, thereby improving our understanding of genotype-phenotype connections. Article summarySingle nucleotide polymorphisms (SNPs), the most common form of genomic variation, drive micro-evolution and adaptation. In Drosophila melanogaster, many SNPs are associated with phenotypes, yet functional validation is rare and experimentally challenging. FlyCADD is a new impact prediction tool that integrates D. melanogaster genome annotations into a single score predicting SNP impact. FlyCADD can be applied to distinguish causal from neutral variants, prioritize variants prior to functional studies, and to interpret natural variation, thereby improving understanding of genotype-phenotype relationships.

genomics↗

Urban sensory conditions alter rival interactions and mate choice in urban and forest tungara frogs

Sexual communication often takes place in networks with multiple competing signalers being simultaneously assessed by mate choosers. Altered sensory conditions, such as noise and light pollution, can affect communication by altering signal production and perception. While evidence of sensory pollution affecting sexual signaling is widespread, few studies assess impacts on sexual signaling during rival interactions as well as mate choice, let alone whether urban and forest populations have diverged in their response. Here, we investigate the effects of urban sensory conditions on sexual communication in urban and forest tungara frogs (Engystomops pustulosus). We recorded dyadic vocal rival interactions and assessed mate choice with and without noise and light pollution in the lab. We show that urban sensory conditions can directly impact the intensity of rival interactions, differences between rivals and mate choice, though changes were often in opposite directions for frogs of urban and forest origins. Moreover, we demonstrate that changes in rival interactions in response to light and noise pollution can also indirectly affect how females choose between potential mates. Our study reveals origin-dependent direct and indirect effects of noise and light pollution, which ultimately translate into fitness consequences for sexual communication in urban populations.

animal behavior and cognition↗

Tetrapod vocal evolution: higher frequencies and faster rates of evolution in mammalian vocalizations

Using the voice to produce sound is a widespread form of communication and plays an important role in contexts as diverse as parent-offspring interactions and courtship. Variation in the tempo and mode of vocal signal evolution has been studied in a phylogenetic context within orders or classes, but understanding vocal signal evolution ultimately requires comparison across all major lineages involved. Here we used comparative analyses to investigate the evolution of dominant frequency (i.e., the frequency with the highest energy content) and its association with body weight across 873 species of mammals, birds and frogs. In agreement with previous studies, we found that the negative allometric relationship between body weight and vocal frequency is a general feature of vocal systems. In addition, we found mammals to consistently vocalize at higher frequencies, and evolved their vocalizations at around 6-fold faster rates than those of birds and frogs. Although all three groups strongly rely on vocal communication, our findings show that only mammals have extensively explored the spectral acoustic space. We argue that such high vocal diversity of mammals is made possible by their unique hearing system, which evolved in the context of a small, parental-caring, nocturnal and insectivore ancestor, and has allowed them to detect, and therefore to evolve, a richer array of frequencies than other tetrapods.

evolutionary biology↗

Predicting and quantifying coexistence outcomes between resident and invading species using trait and abundance data

A major challenge in invasion ecology is determining which introduced species pose a threat to resident species through competitive displacement. Here, we provide a statistical framework rooted in coexistence theory to calculate coexistence outcomes - including competitive displacement - between resident and invading species. Advantageously, our framework uses readily available trait and abundance data rather than the demographic data traditionally used in coexistence theory applications which is often difficult to collect for most species. Our framework provides methods for predicting displacement that has yet to manifest in incipient invasions, and for quantifying displacement in ongoing invasions. We apply this framework to the native and introduced gecko species on Curacao and predict the displacement of all three native species by introduced species and quantify that the displacement of one native species is already underway. Our results affirm that trait and abundance data are suitable proxies to reasonably predict and quantify coexistence outcomes.

ecology↗

Elevated human footprint on islands promotes both introduction and extinction probability of insular reptiles at opposite ends of geographic, evolutionary and ecological continua

Species ranges are changing in the Anthropocene, the ranges of introduced species are expanding, while extinction-prone species are contracting. Introductions and extinctions are both caused by how species respond to human impacts, but it is unknown why the ranges of some species expand and some contract. Here, we test that this opposite response of human impact is due to introduced and extinction-prone species falling at opposite ends of geographic, evolutionary, or ecological trait continua. We constructed a database of native range maps, traits, phylogenetic relationships, and the introduction and extinction-prone status of squamate reptiles with ranges native to the Western Hemisphere. Across >3,000 snake and lizard species (88% of known native squamates), 142 had been introduced elsewhere and 483 were extinction-prone (i.e., extinct, vulnerable, threatened). To explain variation in status, we first tested if the same human-impacted regions in the Americas contained the native ranges of species of either status. Second, we tested for phylogenetic signal in species status. Finally, we tested the explanatory power of multiple trait continua. The native ranges of introduced and extinction-prone reptiles were clustered in island regions with high human impact vs. mainland regions with lower human impact. Phylogenetic signal was weak for status, but introduced and extinction-prone species were clustered in different clades. All geographic and ecological traits that explained both statuses supported the opposite ends hypothesis. Introduced species had larger, edgier ranges, while extinction-prone species had smaller, simpler ranges. Introduced species were mostly herbivorous/omnivorous, while extinction-prone species were mostly carnivorous. Introduced species produced larger clutches, while extinction-prone species were smaller in body size. In the Anthropocene, the naive ranges of introduced and extinction-prone species are in the same human-impacted regions where trait continua, having opposite effects, determine whether species ranges expand or contract in the continuing face of global change.

ecology↗

Genomic evidence of paternal genome elimination in globular springtails

AO_SCPLOWBSTRACTC_SCPLOWPaternal genome elimination (PGE) - a type of reproduction in which males inherit but fail to pass on their fathers genome - evolved independently in six to eight arthropod clades. Thousands of species, including several important for agriculture, reproduce via this mode of reproduction. While PGE is well established in some of the clades, the evidence in globular springtails (Symphypleona) remains elusive, even though they represent the oldest and most species rich clade putatively reproducing via PGE. We sequenced genomic DNA from whole bodies of Allacma fusca males with high fractions (>27.5%) of sperm to conclusively confirm that all the sperm carry one parental haplotype only. Although it is suggestive that the single haplotype present in sperm is maternally inherited, definitive genetic proof of the parent of origin is still needed. The genomic approach we developed allows for detection of genotypic differences between germline and soma in all species with sufficiently high fraction of germline in their bodies. This opens new opportunities for scans of reproductive modes in small organisms.

genomics↗

Population genetic bottleneck has only marginal effects on fitness evolution and its repeatability in dioecious C. elegans

The predictability of evolution is expected to depend on the relative contribution of deterministic and stochastic processes. This ratio is modulated by effective population size. Smaller effective populations harbor less genetic diversity and stochastic processes are generally expected to play a larger role, leading to less repeatable evolutionary trajectories. Empirical insight into the relationship between effective population size and repeatability is limited and focused mostly on asexual organisms. Here, we tested whether fitness evolution was less repeatable after a population bottleneck in obligately outcrossing populations of Caenorhabditis elegans. Replicated populations founded by 500, 50, or 5 individuals (no/moderate/strong bottleneck) were exposed to a novel environment with a different bacterial prey. As a proxy for fitness, population size was measured after one week of growth before and after 15 weeks of evolution. Surprisingly, we found no significant differences among treatments in their fitness evolution. Even though the strong bottleneck reduced the relative contribution of selection to fitness variation, this did not translate to a significant reduction in the repeatability of fitness evolution. Thus, although a bottleneck reduced the contribution of deterministic processes, we conclude that the predictability of evolution may not universally depend on effective population size, especially in sexual organisms.

evolutionary biology↗

Environmental and morphological constraints interact to drive the evolution of communication signals in frogs

Animals show a rich diversity of signals and displays. Among the many selective forces driving the evolution of communication between individuals, one widely recognized factor is the structure of the environment in which signals are produced, transmitted and received. In particular, animals communicating by sounds often emit acoustic signals from specific locations, such as high up in the air, from the ground or in the water. The properties of these different display sites will impose different constraints on sound production and transmission and may therefore drive signal evolution. Here, we used comparative phylogenetic analyses to assess the relationship between the display site properties and the structure of reproductive calls from 161 frog species from the frog families Ranidae, Leptodactylidae and Hylidae. Specifically, we compared the dominant frequency of species that vocalize from aquatic versus non-aquatic sites, and its relation with body size. We found that the dominant frequency of frogs calling from the water was lower than that of species calling outside of the water, a trend that was consistent across the three families studied. Furthermore, phylogenetic path analysis revealed that the call site had both direct and indirect effects on the dominant frequency. Indirect effects were mediated by call site influencing male body size, which in turn was negatively associated to call dominant frequency. Our results suggest that properties of display sites can drive signal evolution, most likely through morphological constraints, in particular the ones imposed on the sound production mechanism. Also, variation in body size between calling sites explained some of the differences we found in call frequency, highlighting the relevance of the interplay between morphological adaptation and signal evolution. Changes of display site may therefore have important evolutionary consequences, as it may influence sexual selection processes and ultimately may even promote speciation. Impact summaryTo attract or impress mates, animals have evolved a great diversity of communication signals, such as song and dance, or brightly colored body parts. Whether these sexual signals are successful depends to a large extent on the environment in which they are produced, transmitted and perceived. For acoustic signals, such as the mating calls of frogs, the environment is well known to influence both their transmission and perception. The impact of the environment on the production of sounds is however far less understood. Here we studied the relation between the environment and signal design across a wide range of frog species, specifically comparing calls of aquatic versus non-aquatic species. Frogs that called from water were found to call at lower pitch, which was partly explained by the fact that they were also larger. Our results point towards an important environmental driver of signal evolution, namely morphological constraints on signal production. We argue that the environment can impose limits on morphological traits that are either directly or indirectly involved in signal production. Such a mechanism would in particular be important when species move into new habitats, as rapid changes to display sites may lead to rapid changes in sexual signaling and sexual attractiveness.

evolutionary biology↗

Lipids as currency in ecological interactions: Competition and facilitation between two lipid scavenging parasitoids

Interspecific interactions in nature often revolve around the acquisition of nutrients. Depending on the organisms metabolic requirements, competition for specific essential nutrients may occur, which selects for increased abilities to monopolize, consume and store these nutrients. Lipid scavengers are organisms that rely on exogenous lipid acquisition as they lack the ability to synthesize fatty acids de novo or in sufficient quantity. Most parasitoid insects are lipid scavengers: they obtain all required lipids by feeding on their hosts as larvae. Here we study the nutritional ecology of competitive interactions between native Nasonia vitripennis and introduced Tachinaephagus zealandicus. While the former was already known to lack lipogenesis, we show that T. zealandicus also relies on host lipids. The interactions between the two species were studied using competition experiments, in which oviposition of T. zealandicus on a host was followed by multiparasitism by N. vitripennis. The outcome of competition was determined by the duration of the time lag between oviposition events. N. vitripennis was superior when arriving 3 days after oviposition by T. zealandicus. In contrast, 9 days after oviposition of T. zealandicus we observed complete reversal, and no N. vitripennis offspring were able to develop. Only when N. vitripennis laid eggs 15 days after T. zealandicus oviposition, both species could emerge from the same host. However, N. vitripennis realizes only 10% of its potential fitness at this time point because prior parasitization by the gregarious T. zealandicus compartmentalizes the host resources, limiting the spread of N. vitripennis venom. This study shows that successful reproduction of N. vitripennis at 15 days was achieved by hyperparasitizing, a capability that provides a fitness benefit to N. vitripennis, as it extends the time window that hosts are available for parasitization. Choice tests with hosts at different time intervals after T. zealandicus oviposition revealed a partial mismatch in N. vitripennis females between competition avoidance and offspring performance, which may be linked to the limited co-evolutionary time between native and introduced species. We discuss our results in the context of nutritional ecology and, specifically, the role of lipids in ecological interactions.

ecology↗

Parallel evolution in the integration of a co-obligate aphid symbiosis

Insects evolve dependencies - often extreme - on microbes for nutrition. These include cases where insects harbour multiple endosymbionts that function collectively as a metabolic unit. How do these metabolic co-dependencies originate, and is there a predictable sequence of events leading to the integration of new symbionts? While dependency on multiple nutrient-provisioning symbionts has evolved numerous times across sap-feeding insects, there is only one known case of metabolic co-dependency in aphids, between Buchnera aphidicola and Serratia symbiotica in the Lachninae subfamily. Here we identify three additional independent transitions to the same co-obligate symbiosis in different aphids. A comparison of recent and ancient associations allows us to investigate intermediate stages of metabolic and physical integration between the typically facultative symbiont, Serratia, and the ancient obligate symbiont Buchnera. We find that these uniquely replicated evolutionary events support the idea that co-obligate associations initiate in a predictable manner, through parallel evolutionary processes. Specifically, we show (i) how the repeated losses of the riboflavin pathway in Buchnera leads to dependency on Serratia, (ii) evidence of a stepwise process of symbiont integration, whereby dependency evolves first, then essential amino acid pathways are lost (at ~30-60MYA), which coincides with increased physical integration of the companion symbiont; and (iii) dependency can evolve prior to specialised structures (e.g. bacteriocytes), and in one case with no direct nutritional basis. More generally, our results suggest the energetic costs of synthesising nutrients may provide a unified explanation for the sequence of gene loses that occur during the evolution of co-obligate symbiosis.

evolutionary biology↗

Gene regulatory mechanisms underlying the evolutionary loss of a polygenic trait

Trait loss is a pervasive phenomenon in evolution, yet the underlying molecular causes have been identified in only a handful of cases. Most of these involve loss-of-function mutations in one or more trait-specific genes. Parasitoid insects are fatty acid auxotrophs: they lost the ability to convert dietary sugars into fatty acids, a trait that is ubiquitous among non-parasitoid animals and is enabled by a highly conserved set of genes. Earlier research suggests that lack of lipogenesis is caused by changes in gene regulation, rather than gene decay. We compared transcriptome-wide responses to sugar-feeding in the non-lipogenic parasitoid species Nasonia vitripennis and the lipogenic Drosophila melanogaster. Both species adjusted their metabolism within four hours after feeding, but there was little overlap at the gene level between the responses of the two species. Even at the pathway-level, there were sharp differences between the expression profiles of the two species, especially in carbohydrate and lipid metabolic pathways. Several genes coding for key enzymes in acetyl-CoA metabolism, such as malonyl-CoA decarboxylase (MCD) and HMG-CoA synthase differed in expression between the two species. Their combined action likely blocks lipogenesis in the parasitoid species. Network analysis indicates most genes involved in these pathways to be highly connected, which suggest they have pleiotropic effects and could explain the absence of gene degradation. Our results indicate that modification of expression levels of only a few non-connected genes, such as MCD, is sufficient to enable complete loss of lipogenesis in N. vitripennis.

evolutionary biology↗

Genomic resources for Goniozus legneri, Aleochara bilineata and Paykullia maculata, representing three independent origins of the parasitoid lifestyle in insects

Parasitoid insects are important model systems for a multitude of biological research topics and widely used as biological control agents against insect pests. While the parasitoid lifestyle has evolved numerous times in different insect groups, research has focused almost exclusively on Hymenoptera from the parasitica clade. The genomes of several members of this group have been sequenced, but no genomic resources are available from any of the other, independent evolutionary origins of the parasitoid lifestyle. Our aim here was to develop genomic resources for three parasitoid insects outside the parasitica. We present draft genome assemblies for Goniozus legneri, a parasitoid Hymenopteran more closely related to the non-parasitoid wasps and bees than to the parasitica wasps, the Coleopteran parasitoid Aleochara bilineata and the Dipteran parasitoid Paykullia maculata. The genome assemblies are fragmented, but complete in terms of gene content. We also provide preliminary structural annotations. We anticipate that these genomic resources will be valuable for testing the generality of findings obtained from parasitica wasps in future comparative studies.\n\nData availabilityThe Whole Genome Shotgun projects have been deposited at DDBJ/ENA/GenBank under the accessions NCVS00000000 (G. legneri), NBZA00000000 (A. bilineata) and NDXZ00000000 (P. maculata). The versions described in this paper are versions NCVS01000000, NBZA01000000 and NDXZ01000000, respectively. Mapped reads and genome annotations are available through http://parasitoids.labs.vu.nl/parasitoids/. This website also includes genome browsers and viroblast instances for each genome.

genomics↗