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Hrcek, J.

Publications and source records attributed to Hrcek, J..

12 recordsLinked to original sources

Selection history alters fitness across ecological interactions in a fly-parasitoid system

Species interactions shape ecological dynamics, but adaptation to one interaction can trade off with others. Experiments that measure such evolved fitness changes across multiple interactions remain rare. We used experimental evolution to test whether recent selection under one ecological interaction changes fitness under other interactions in a fly-parasitoid system. We evolved a genetically diverse Drosophila melanogaster population for 15-17 generations under three regimes: benign conditions (control), high intraspecific competition, and infection by the parasitoid wasp Leptopilina boulardi. We then measured fly fitness (egg-to-adult survival and subsequent reproduction) under benign conditions, high intraspecific competition, and infection by three other parasitoid species and an additional conspecific L. boulardi strain. Selection history strongly influenced fitness across interactions. Populations maintained under high larval density showed reduced survival under infection by L. boulardi and L. victoriae, indicating a trade-off between past selection for competition and defence against some parasitoids. Populations evolved under parasitoid infection by L. boulardi showed increased resistance to a conspecific strain but reduced fitness when infected by another species, L. heterotoma. Our results show that rapid evolution in response to a single interaction can reshape multiple ecological interactions through fitness trade-offs, highlighting how recent evolutionary history may influence community dynamics and invasion susceptibility.

evolutionary biology↗

Spatial turnover amplifies with trophic level in hyperdiverse food webs

One of the most intuitive ideas in ecology is that diversity at lower trophic levels in food webs provides niches to support diversity at higher trophic levels. This accumulation of diversity can be limited by survival of species in the landscape, but revealing these limits has been challenging. We analyze spatial turnover in a hyperdiverse parasitoid-caterpillar-plant food web across 75,000 km2 of continuous lowland rainforest in Papua New Guinea. Species turnover across sites is higher in parasitoids than in their caterpillar hosts. Furthermore, turnover of interactions is also higher in parasitoid-caterpillar than caterpillar-plant networks. Spatial turnover thus amplifies upwards across trophic levels, forcing parasitoids to live closer to spatial persistence limits. Consequently, progressing rainforest fragmentation can especially endanger parasitoids.

ecology↗

Dating the origin of a viral domestication event in parasitoid wasps attacking Diptera

Over the course of evolution, hymenopteran parasitoids have developed a close relationship with heritable viruses, sometimes even integrating viral genes into their chromosomes. For example, in Drosophila parasitoids belonging to the Leptopilina genus, 13 viral genes from the Filamentoviridae family have been integrated and domesticated to deliver immunosuppressive factors to host immune cells, thereby protecting parasitoid offspring from host immune responses. The present study aims to comprehensively characterise this domestication event in terms of the viral genes involved, the wasp diversity affected by this event, and its chronology. Our genomic analysis of 41 Cynipoidea wasps from six subfamilies revealed 18 viral genes that were endogenised during the early radiation of the Eucoilini+Trichoplastini clade around 75 million years ago. Wasps from this highly diverse clade develop not only from Drosophila but also from a variety of Schizophora. This event coincides with the radiation of Schizophora, a highly speciose Diptera clade, suggesting that viral domestication facilitated wasp diversification in response to host diversification. Additionally, at least one viral gene was replaced by another Filamentovirus gene in one of the species, highlighting the dynamic nature of viral endogenisation. This study highlights the impact of viral domestication on the diversification of parasitoid wasps.

evolutionary biology↗

Single-fly assemblies fill major phylogenomic gaps across the Drosophilidae Tree of Life

Long-read sequencing is driving rapid progress in genome assembly across all major groups of life, including species of the family Drosophilidae, a longtime model system for genetics, genomics, and evolution. We previously developed a cost-effective hybrid Oxford Nanopore (ONT) long-read and Illumina short-read sequencing approach and used it to assemble 101 drosophilid genomes from laboratory cultures, greatly increasing the number of genome assemblies for this taxonomic group. The next major challenge is to address the laboratory culture bias in taxon sampling by sequencing genomes of species that cannot easily be reared in the lab. Here, we build upon our previous methods to perform amplification-free ONT sequencing of single wild flies obtained either directly from the field or from ethanol-preserved specimens in museum collections, greatly improving the representation of lesser studied drosophilid taxa in whole-genome data. Using Illumina Novaseq X Plus and ONT P2 sequencers with R10.4.1 chemistry, we set a new benchmark for inexpensive hybrid genome assembly at US $150 per genome while assembling genomes from as little as 35 ng of genomic DNA from a single fly. We present 183 new genome assemblies for 179 species as a resource for drosophilid systematics, phylogenetics, and comparative genomics. Of these genomes, 62 are from pooled lab strains and 121 from single adult flies. Despite the sample limitations of working with small insects, most single-fly diploid assemblies are comparable in contiguity (>1Mb contig N50), completeness (>98% complete dipteran BUSCOs), and accuracy (>QV40 genome-wide with ONT R10.4.1) to assemblies from inbred lines. We present a well-resolved multi-locus phylogeny for 360 drosophilid and 4 outgroup species encompassing all publicly available (as of August 2023) genomes for this group. Finally, we present a Progressive Cactus whole-genome, reference-free alignment built from a subset of 298 suitably high-quality drosophilid genomes. The new assemblies and alignment, along with updated laboratory protocols and computational pipelines, are released as an open resource and as a tool for studying evolution at the scale of an entire insect family.

evolutionary biology↗

Warming decreases host survival with multiple parasitoids, but parasitoid performance also decreases

Current global changes are reshaping ecological communities and modifying environmental conditions. We need to recognize the combined impact of these biotic and abiotic factors on species interactions, community dynamics, and ecosystem functioning. Specifically, the strength of predator-prey interactions often depends on the presence of other natural enemies: it weakens with competition and interference or strengthens with facilitation. Such effects of multiple predators on prey are likely to be affected by changes in the abiotic environment, altering top-down control, a key structuring force in natural and agricultural ecosystems. Here, we investigated how warming alters the effects of multiple predators on prey suppression using a dynamic model coupled with empirical laboratory experiments with Drosophila-parasitoid communities. While multiple parasitoids enhanced top-down control under warming, parasitoid performance generally declined when another parasitoid was present due to competitive interactions. This could reduce top-down control over multiple generations. Our study highlights the importance of accounting for interactive effects between abiotic and biotic factors to better predict community dynamics in a rapidly changing world and thus better preserve ecosystem functioning and services such as biological control.

ecology↗

Microbiome structure of a wild Drosophila community along tropical elevational gradients and comparison to laboratory lines

Variation along environmental gradients in host-associated microbial communities is not well understood, compared to free-living microbial communities. Because elevational gradients may serve as natural proxies for climate change, understanding patterns along these gradients can inform our understanding of the threats hosts and their symbiotic microbes face in a warming world. In this study, we analysed bacterial microbiomes from pupae and adults of four Drosophila species native to Australian tropical rainforests. We sampled wild individuals at high and low elevation along two mountain gradients, to determine natural diversity patterns. Further, we sampled laboratory-reared individuals from isofemale lines established from the same localities, to see if any natural patterns are retained in the lab. In both environments, we controlled for diet to help elucidate other deterministic patterns of microbiome composition. We found small but significant differences in Drosophila bacterial community composition across elevation, with some notable taxonomic differences between different Drosophila species and sites. Further, we found that field-collected fly pupae had significantly richer microbiomes than laboratory-reared pupae. We also found similar microbiome composition in both types of provided diet, suggesting that the significant differences found among Drosophila microbiomes are the product of surrounding environments with different bacterial species pools, possibly bound to elevational differences in temperature. Our results suggest that comparative studies between lab and field specimens help reveal the true variability in microbiome communities that can exist within a single species. ImportanceBacteria form microbial communities inside most higher-level organisms, but we know little about how the microbiome varies along environmental gradients and between natural host populations and laboratory colonies. To explore such effects on insect-associated microbiomes, we studied gut microbiome in four Drosophila species over two mountain gradients in tropical Australia. We also compared these data to individuals kept in the laboratory to understand how different settings changed microbiome communities. We found that field sampled individuals had significantly higher microbiome diversity than those from the lab. In wild Drosophila populations, elevation explains a small but significant amount of the variation in their microbial communities. Our study highlights the importance of environmental bacterial sources for Drosophila microbiome composition across elevational gradients, and shows how comparative studies help reveal the true flexibility in microbiome communities that can exist within a species.

ecology↗

Multiple parasitoid species enhance top-down control, but parasitoid performance is context-dependent

O_LIEcological communities are composed of many species, forming complex networks of interactions. Current environmental changes are altering community composition. We thus need to identify which aspects of species interactions are primarily driven by community structure and which by species identity to predict changes in the functioning of communities. Yet, this partitioning of effects is challenging and thus rarely explored. C_LIO_LIHere we disentangled the influence of community structure and the identity of co-occurring species on the outcome of consumer-resource interactions using a host-parasitoid system. C_LIO_LIWe used four community modules that are common in host-parasitoid communities to represent community structure (i.e., host-parasitoid, exploitative competition, alternative host, and a combination of both exploitative competition and alternative host). We assembled nine different species combinations per community module in a laboratory experiment using a pool of three Drosophila hosts and three larval parasitoid species. To investigate the potential mechanisms at play, we compared host suppression and parasitoid performance across community modules and species assemblages. C_LIO_LIWe found that multiple parasitoid species enhanced host suppression due to sampling effect, weaker interspecific than intraspecific competition between parasitoids, and synergism. However, the effects of community structure on parasitoid performance were species-specific and dependent on the identity of co-occurring species. Consequently, multiple parasitoid species generally strengthen top down-control, but the performance of the parasitoids depends on the identity of either the co-occurring parasitoid species, the alternative host species, or both. C_LIO_LIOur results highlight the importance of preserving predator diversity for ecosystem functioning, but also show that other effects depend on community composition, and will therefore be likely altered by current environmental changes. C_LI

ecology↗

DROP: Molecular voucher database for identification of Drosophila parasitoids

Molecular identification is increasingly used to speed up biodiversity surveys and laboratory experiments. However, many groups of organisms cannot be reliably identified using standard databases such as GenBank or BOLD due to lack of sequenced voucher specimens identified by experts. Sometimes a large number of sequences are available, but with too many errors to allow identification. Here we address this problem for parasitoids of Drosophila by introducing a curated open-access molecular reference database, DROP (Drosophila parasitoids). Identifying Drosophila parasitoids is challenging and poses a major impediment to realize the full potential of this model system in studies ranging from molecular mechanisms to food webs, and in biological control of Drosophila suzukii. In DROP (http://doi.org/10.5281/zenodo.4519656), genetic data are linked to voucher specimens and, where possible, the voucher specimens are identified by taxonomists and vetted through direct comparison with primary type material. To initiate DROP, we curated 154 laboratory strains, 856 vouchers, 554 DNA sequences, 16 genomes, 14 transcriptomes, and 6 proteomes drawn from a total of 183 operational taxonomic units (OTUs): 114 described Drosophila parasitoid species and 69 provisional species. We found species richness of Drosophila parasitoids to be heavily underestimated and provide an updated taxonomic catalogue for the community. DROP offers accurate molecular identification and improves cross-referencing between individual studies that we hope will catalyze research on this diverse and fascinating model system. Our effort should also serve as an example for researchers facing similar molecular identification problems in other groups of organisms.

genomics↗

Experimental warming influences species abundances in a Drosophila host community through direct effects on species performance rather than altered competition and parasitism

Current global warming trends are expected to have direct effects on species through their sensitivity to temperature, as well as on their biotic interactions, with cascading indirect effects on species, communities, and entire ecosystems. To predict the community-level consequences of global change we need to understand the relative roles of both the direct and indirect effects of warming. We used a laboratory experiment to investigate how warming affects a tropical community of three species of Drosophila hosts interacting with two species of parasitoids over a single generation. Our experimental design allowed us to distinguish between the direct effects of temperature on host species performance, and indirect effects through altered biotic interactions (competition among hosts and parasitism by parasitoid wasps). Although experimental warming significantly decreased parasitism for all host-parasitoid pairs, the effects of parasitism and competition on host communities did not vary across temperatures. Instead, effects on host relative abundances were species-specific, with one host species dominating the community at warmer temperatures, independently of parasitism and competition treatments. Our results show that temperature shaped a Drosophila host community directly through differences in species thermal performance, and not via its influences on biotic interactions.

ecology↗

Intraspecific variation in symbiont density in an insect-microbe symbiosis

AO_SCPLOWBSTRACTC_SCPLOWMany insects host vertically-transmitted microbes, which can confer benefits to their hosts but are costly to maintain and regulate. A key feature of these symbioses is variation: for example, symbiont density can vary among host and symbiont genotypes. However, the evolutionary forces maintaining this variation remain unclear. We studied variation in symbiont density using the pea aphid (Acyrthosiphon pisum) and the bacterium Regiella insecticola, a symbiont that can protect its host against fungal pathogens. We found that relative symbiont density varies both between two Regiella phylogenetic clades and among aphid biotypes. Higher-density symbiont infections are correlated with stronger survival costs, but variation in density has little effect on the protection Regiella provides against fungus. Instead, we found that in some aphid genotypes, a dramatic decline in symbiont density precedes the loss of a symbiont infection. Together, our data suggest that the optimal density of a symbiont infection is likely different from the perspective of aphid and microbial fitness. Regiella might prevent loss by maintaining high within-host densities, but hosts do not appear to benefit from higher symbiont numbers and may be advantaged by losing costly symbionts in certain environments. The standing variation in symbiont density observed in natural populations could therefore be maintained by antagonistic coevolutionary interactions between hosts and their symbiotic microbes.

evolutionary biology↗

Molecular analyses reveal consistent food web structure with elevation in rainforest Drosophila - parasitoid communities

The analysis of interaction networks across spatial environmental gradients is a powerful approach to investigate the responses of communities to global change. Using a combination of DNA metabarcoding and traditional molecular methods we built bipartite Drosophila-parasitoid food webs from six Australian rainforest sites across gradients spanning 850 m in elevation and 5{degrees} Celsius in mean temperature. Our cost-effective hierarchical approach to network reconstruction separated the determination of host frequencies from the detection and quantification of interactions. The food webs comprised 5-9 host and 5-11 parasitoid species at each site, and showed a lower incidence of parasitism at high elevation. Despite considerable turnover in the relative abundance of host Drosophila species, and contrary to some previous results, we did not detect significant changes to fundamental metrics of network structure including nestedness and specialisation with elevation. Advances in community ecology depend on data from a combination of methodological approaches. It is therefore especially valuable to develop model study systems for sets of closely-interacting species that are diverse enough to be representative, yet still amenable to field and laboratory experiments.

ecology↗

Interacting effects of the abiotic and biotic environment on fitness of rainforest Drosophila

Competition within and between species can have large effects on fitness and may therefore drive local adaptation. However, these effects are rarely tested systematically, or considered when predicting species responses to environmental change. We used a field transplant experiment to test the effects of intra and interspecific competition on fitness across the ecological niches of two rainforest Drosophila species that replace each other along an elevation gradient. For the species with the broader elevational range, we also tested for adaptation to the local abiotic and biotic environment. In both species, intraspecific competition reduced productivity more than interspecific competition at the centre of its elevational range, while interspecific competition had a stronger effect at the range edge, where the competing species is more abundant. Local adaptation was detected in the centre of the range of the more widespread species, but only in the presence of intraspecific competition. This study is the first to demonstrate that fitness effects of inter-specific competition increase at ecological margins, while intra-specific competition has more pervasive effects at range centres. This is a key assumption of "tangled bank" models of community evolution and has important implications for predicting the resilience of ecological networks to global change.

evolutionary biology↗