Biology subjects

Feder, J. L.

Publications and source records attributed to Feder, J. L..

8 recordsLinked to original sources

bioRxiv2025

Rapid evolution of Wolbachia in cherry fruit flies

Wolbachia is a widespread bacterial endosymbiont in arthropods known for its ability to manipulate host reproduction through cytoplasmic incompatibility (CI), thereby promoting its spread. However, Wolbachia harbors an array of mobile genetic elements (MGEs) that can rapidly alter its genomic structure and content, including the cif loci responsible for CI. At the phylogenetic scale, Wolbachia genomes are shown to be dynamic with MGEs causing widespread genome rearrangements. But on ecological time scales, the evolution of Wolbachia remains largely unknown. In this study, we leverage the natural history of Wolbachia in cherry-infesting fruit flies in the Rhagoletis cingulata sibling species group. Members of this species group share a common Wolbachia strain, wCin2, and their divergence spans from 1,000 to 150,000 years ago. We utilized Nanopore sequencing to characterize wCin2 Wolbachia genome divergence across recent to more distant evolutionary timescales. We report rapid evolution of population-level differences in gene content (including cif loci and MGEs) and genome structure, with differentiation increasing with time since host divergence. Notably, structural variants were the first to appear both between and among wCin2 populations. Our results also indicated that the CI phenotype previously attributed to a distinct Wolbachia strain, wCin3, that coinfects flies in the southwestern USA and Mexico, may instead be caused by cif genes that were horizontally transferred into wCin2. Finally, we discovered a novel Wolbachia strain, wInd, which appears to have been recently horizontally acquired by cherry fly populations in the Pacific Northwest of the USA. Our findings underscore the fluidity and rapid genome evolution of Wolbachia, with significant implications for cif gene dynamics and potential impacts on host evolutionary trajectories. Author SummaryIn our study, we explore the genome evolution of Wolbachia, a common bacterial endosymbiont found in many insects that can manipulate its hosts reproduction to help it spread more effectively. Wolbachias genome is shown to change dramatically over long evolutionary periods due to mobile genetic elements. However, little is known about how Wolbachias genome evolves over shorter ecological timeframes. Here, we utilized cherry-infesting fruit flies and their Wolbachia strain known as wCin2, both of which have spread across North America for the past 150,000 years. Using long-read sequencing, we assembled multiple wCin2 Wolbachia genomes from across North America and made comparisons between wCin2 Wolbachia genomes that have recently diverged and comparisons to those that have been isolated for over 150,000 years. Our findings reveal that Wolbachias genome can evolve swiftly, with differences in gene content and most prominently genome structure arising between recently separated Wolbachia populations and increasing as populations diverge over time. Interestingly, these changes also impact the key genes responsible for Wolbachias reproductive manipulation. This research highlights the rapid and dynamic nature of Wolbachia genome evolution across different evolutionary timescales and offers insights into endosymbiont-host relationships as well as their potential impact on host speciation and vector control.

evolutionary biology↗

bioRxiv2023

Cold tolerance and diapause within across trophic levels: endoparasitic wasps and their fly host have similar phenotypes

Low temperatures associated with winter can limit the survival of organisms, especially ectotherms whose body temperature is similar to their environment. Important adaptations for overwintering such as cold hardiness and diapause have been well-explored in many insect taxa. However, there is a gap in understanding how overwintering may vary among groups of species that interact closely, such as multiple parasitoid species that attack the same host insect. Our study investigated cold tolerance and diapause phenotypes in three endoparasitoid wasps of the apple maggot fly Rhagoletis pomonella (Diptera: Tephritidae): Utetes canaliculatus, Diachasma alloeum, and Diachasmimorpha mellea (Hymenoptera: Braconidae). Using a combination of respirometry and eclosion tracking, we detected diapause phenotypes in all three wasp species, remarkably similar to the fly host. Weak diapause was rare (< 5%) in all three wasp species, and while most D. mellea (93%) entered prolonged diapause under warm conditions, the majority of U. canaliculatus (92%) and D. alloeum (72%) averted diapause (non-diapause). There was limited interspecific variation in acute cold tolerance among the three wasp species: wasps and flies had similarly high survival (>87%) following exposure to extreme low temperatures (- 20{degrees}C) as long as their body fluids did not freeze. The wasp species showed little interspecific variation in survival following prolonged exposure to mild chilling of 8 or more weeks at 4{degrees}C. This study shows remarkable conservation of cold tolerance and diapause phenotypes within and across trophic levels. The interaction between diapause phenotype and cold hardiness in these parasitoids is an interesting direction for future research. Graphical Abstract and Highlights O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=133 SRC="FIGDIR/small/522725v1_ufig1.gif" ALT="Figure 1"> View larger version (23K): org.highwire.dtl.DTLVardef@826a3aorg.highwire.dtl.DTLVardef@c3963org.highwire.dtl.DTLVardef@8baa33org.highwire.dtl.DTLVardef@1530d03_HPS_FORMAT_FIGEXP M_FIG C_FIG O_LIThe apple maggot fly and its parasitoids exhibit the same three diapause phenotypes C_LIO_LIEach parasitoid wasp species exhibits different proportions of these phenotypes C_LIO_LIUtetes canaliculatus and Diachasma alloeum are freeze-avoidant, like their host fly C_LIO_LIThese wasps and flies survive to similarly extreme low temperatures (c. -20{degrees}C) C_LIO_LIEach wasp species survives prolonged exposure to mild chilling (4{degrees}C) similarly well C_LI

physiology↗

bioRxiv2022

Simulated climate change causes asymmetric responses in insect life history timing potentially disrupting a classic ecological speciation system

Climate change may alter phenology within populations with cascading consequences for community interactions and on-going evolutionary processes. Here, we measured the response to climate change in two sympatric, recently diverged (~170 years) populations of Rhagoletis pomonella flies specialized on different host fruits (hawthorn and apple) and their parasitoid wasp communities. We tested whether warmer temperatures affect dormancy regulation and its consequences for synchrony across trophic levels and temporal isolation between divergent populations. Under warmer temperatures, both fly populations developed earlier. However, warming significantly increased the proportion of maladaptive pre-winter development in apple, but not hawthorn, flies. Parasitoid phenology was less affected, potentially generating ecological asynchrony. Observed shifts in fly phenology under warming may decrease temporal isolation, potentially limiting on-going divergence. Our findings of complex sensitivity of life-history timing to changing temperatures predict that coming decades may see multifaceted ecological and evolutionary changes in temporal specialist communities.

ecology↗

bioRxiv2021

Connecting neuromodulation, brain development, and life history timing associated with ecological speciation in Rhagoletis pomonella

Host shifts are considered a key generator of insect biodiversity. For insects, adaptation to new host plants often requires changes in larval/pupal development and behavioural preference towards new hosts. Neurochemicals play key roles in both development and behaviour, and therefore provide a potential source for such synchronization. Here, we correlated life history timing, brain development, and corresponding levels of 14 neurochemicals in Rhagoletis pomonella (Diptera: Tephritidae), a species undergoing ecological speciation through an ongoing host shift from hawthorn to apple fruit. These races exhibit differences in pupal diapause timing as well as adult behavioural preference with respect to their hosts. This difference in behavioral preference is coupled with differences in neurophysiological response to host volatiles. We found that apple race pupae exhibited adult brain morphogenesis three weeks faster after an identical simulated winter than the hawthorn race, which correlated with significantly lower titres of several neurochemicals. In some cases, particularly biogenic amines, differences in titres were reflected in the mature adult stage, when host preference is exhibited. In summary, life history timing, neurochemical titre, and brain development can be coupled in this speciating system, providing new hypotheses for the origins of new species through host shifts.

ecology↗

bioRxiv2020

Assessing the role of inversions in maintaining genomic differentiation after secondary contact: local adaptation, genetic incompatibilities, and drift

Due to their effects on reducing recombination, chromosomal inversions may play an important role in speciation by establishing and/or maintaining linked blocks of genes causing reproductive isolation (RI) between populations. These views fit empirical data indicating that inversions typically harbour loci involved in RI. However, previous computer simulations of infinite populations with 2-4 loci involved in RI implied that, even with gene flux as low as 10-8 between alternative arrangements, inversions may not have large, qualitative advantages over collinear regions in maintaining population differentiation after secondary contact. Here, we report that finite population sizes can help counteract the homogenizing consequences of gene flux, especially when several fitness-related loci reside within the inversion. In these cases, the persistence time of differentiation after secondary contact can be similar to when gene flux is absent, and notably longer than the persistence time without inversions. Thus, despite gene flux, population differentiation may be maintained for up to 100,000 generations, during which time new incompatibilities and/or local adaptations might accumulate and facilitate progress towards speciation. How often these conditions are met in nature remains to be determined.

evolutionary biology↗

bioRxiv2020

The genomics of trait combinations and their influence on adaptive divergence

Understanding rapid adaptation requires quantifying natural selection on traits and elucidating the genotype-phenotype relationship for those traits. However, recent studies have often failed to predict the direction of adaptive allelic variation in natural populations from laboratory studies. Here, we test for genomic signatures of genetic correlations to illustrate how multifarious, correlational selection may drive counterintuitive patterns of population divergence in the apple maggot fly, Rhagoletis pomonella (Diptera: Tephritidae). Apple-infesting populations with relatively early emerging adults have recently evolved from hawthorn-infesting populations consisting of relatively later emerging adults. Multiple studies have reported a paradoxical relationship between population differentiation and seasonal timing, as determined by the timing of diapause termination; alleles associated with late termination occur at higher frequencies in the earlier emerging apple-infesting populations compared to hawthorn-infesting populations. We present evidence that historical selection on diapause termination and another trait, initial diapause intensity, over geographic gradients generated genetic correlations between the traits in a direction antagonistic to contemporary selection on apple-infesting populations. Single nucleotide polymorphism in genomic regions of high linkage disequilibrium associated strongly with diapause termination and intensity, population divergence, geography, and evolutionary responses in laboratory selection experiments. These associations were consistent with geographically variable selection and with correlated evolutionary responses driving higher frequencies of late-associated alleles in the early emerging apple race. In contrast, loci associated only with diapause termination showed the expected pattern (more early-associated alleles in the apple race) in half of the population pairs. Our results suggest that selection on loci demonstrating antagonistic pleiotropy may often shape genomic footprints of rapid adaptation.

evolutionary biology↗

bioRxiv2020

A rapidly evolved shift in life history timing during ecological speciation is driven by the transition between developmental phases

For insect species in temperate environments, seasonal timing is often governed by the regulation of diapause, a complex developmental program that allows insects to weather unfavorable conditions and synchronize their lifecycles with available resources. Diapause consists of a series of phases that govern initiation, maintenance, and termination of this developmental pathway. The evolution of insect seasonal timing depends in part on how these phases of diapause development and post-diapause development interact to affect variation in phenology. Here, we dissect the physiological basis of a recently evolved phenological shift in Rhagoletis pomonella (Diptera: Tephritidae), a model system for ecological divergence. A recently derived population of R. pomonella shifted from specializing on native hawthorn fruit to earlier fruiting introduced apples, resulting in a 3-4 week shift in adult emergence timing. We tracked metabolic rates of individual flies across post-winter development to test which phases of development may act either independently or in combination to contribute to this recently evolved divergence in timing. Apple and hawthorn flies differed in a number of facets of their post-winter developmental trajectories. However, divergent adaptation in adult emergence phenology in these flies was due almost entirely to the end of the pupal diapause maintenance phase, with post-diapause development having a very small effect. The relatively simple underpinnings of variation in adult emergence phenology suggest that further adaptation to seasonal change in these flies for this trait might be largely due to the timing of diapause termination unhindered by strong covariance among different components of post-diapause development. Data accessibilityAll data (in the form of tables of all metabolic rate measurements for all individual flies in the study) will be available on DRYAD when the manuscript is published.

evolutionary biology↗

bioRxiv2019

Genome of the parasitoid wasp Diachasma alloeum, an emerging model for ecological speciation and transitions to asexual reproduction

Parasitoid wasps are among the most speciose animals, yet have relatively few available genomic resources. We report a draft genome assembly of the wasp Diachasma alloeum (Hymenoptera: Braconidae), a host-specific parasitoid of the apple maggot fly Rhagoletis pomonella (Diptera: Tephritidae) and a developing model for understanding how ecological speciation can "cascade" across trophic levels. Identification of gene content confirmed the overall quality of the draft genome, and we manually annotated [~]400 genes as part of this study, including those involved in oxidative phosphorylation, chemosensation, and reproduction. Through comparisons to model hymenopterans such as the European honeybee Apis mellifera and parasitoid wasp Nasonia vitripennis, as well as a more closely related braconid parasitoid Microplitis demolitor, we identified a proliferation of transposable elements in the genome, an expansion of chemosensory genes in D. alloeum and other parasitoid wasps, and the maintenance of several key genes with known roles in sexual reproduction and sex determination. The D. alloeum genome will provide a valuable resource for comparative genomics studies in Hymenoptera as well as specific investigations into the genomic changes associated with ecological speciation and transitions to asexuality.

genomics↗