Biology subjects

de Roode, J. C.

Publications and source records attributed to de Roode, J. C..

7 recordsLinked to original sources

bioRxiv2024

The role of a non-native host plant in altering the seasonal dynamics of monarch development

The development and life history of many organisms have evolved to align with annual seasonal changes, but anthropogenic ecological changes have started to disrupt phenological dynamics. To understand the implications of these changes, tractable model systems are needed to identify the causes and consequences of phenological-seasonal asynchrony. Here, we investigate the potential of a non-native and tropical host plant whose phenology has been tuned to different seasonal dynamics to influence the seasonal developmental dynamics of the migratory monarch butterfly Danaus plexippus. Consistent with predictions, we found that the non-native host plant facilitated successful monarch development later into the fall and early winter, which is typically the season North American monarchs enter reproductive diapause and migrate to over-wintering locations. Furthermore, we found evidence that this success could partly be attributed to decreased thermal constraints on development experienced by monarchs reared on A. curassavica.

ecology↗

bioRxiv2024

Extensive transcriptional differentiation and specialization of a parasite across its host's metamorphosis

Foundational theory on life cycle evolution suggests that given genetic independence, the phenotypes presented by different life stages will diverge more when they occupy more dissimilar niches. When divergence between stages is significant and punctual, we typically consider the life cycle complex. In parasites, the delineation between simple and complex life cycles is usually made between those that occupy single and multiple host species. However, many parasites can experience significant niche shifts in a single host. To explore the potential for a hosts metamorphosis to shape divergence between stages across its parasites life cycle, we quantified the transcriptional differentiation and specialization that the protozoan parasite Ophryocystis elektroscirrha exhibits across the metamorphosis of its host the monarch butterfly. We found evidence that O. elektroscirrha differentiates in concordance with the ecological turnover imposed by monarch transitions to different stages, and that patterns of transcriptional decoupling across the O. elektroscirrha exceeded even that of its host. However, because of its greater gene content, the monarch exhibited greater total transcriptional turnover than its parasite. These findings highlight that synthesis of evolutionary theory pertaining to free-living and parasitic life cycles could be facilitated by more nuanced and continuous descriptions of life cycle complexity.

evolutionary biology↗

bioRxiv2024

The role of gene duplication in facilitating divergent patterns of gene expression across a complex life cycle

Explaining the processes that facilitate divergence in the morphologies and functions expressed by organisms throughout their life cycles is fundamental for understanding life cycle evolution. Theory suggests that the expression of traits is decoupled across life stages, thus allowing for evolutionary independence. Although trait decoupling between stages has been described in many studies, explanations of how said decoupling evolves have seldom been considered. Here, we propose evolutionary divergence between duplicate genes as an important mechanism by which life cycle complexity evolves. Because the different phenotypes expressed by organisms throughout their life cycles are coded by the same genome, trait decoupling between stages must be mediated through their divergence in gene expression. Gene duplication has been identified as an important mechanism that enables divergence in gene function and expression between cells and tissues. Here, we examined the temporal changes in gene expression across the monarch butterfly (Danaus plexippus) metamorphosis. We found that within homologous groups, more phylogenetic divergent genes exhibited more distinct temporal expression patterns, and that this relationship scaled such that more phylogenetically diverse homologous groups showed more diverse patterns of gene expression. Furthermore, we found that duplicate genes showed increased stage-specificity relative to singleton genes. Overall, our findings suggest an important role of gene duplication in the evolution of trait decoupling across complex life cycles. SignificanceThe proliferation of many of the worlds most diverse groups of eukaryotes is frequently attributed to their life cycle complexity. By allowing organisms to express different traits throughout their lives, complex life cycles enable individuals to utilize multiple ecological niches. However, the mechanisms that facilitate life cycle evolution are not well understood. We drew inspiration from studies on functional divergence between different tissues and examined the role of gene duplication in generating different patterns of gene expression between stages across the metamorphosis of Danaus plexippus (the monarch butterfly). Our findings suggest that the role of gene duplication in generating differences between cell and tissue types likely extends to trait differentiation between stages within complex life cycles.

evolutionary biology↗

bioRxiv2023

Genome sequence of Ophryocystis elektroscirrha, an apicomplexan parasite of monarch butterflies: cryptic diversity and response to host-sequestered plant chemicals

Apicomplexa are ancient and diverse organisms which have been poorly characterized by modern genomics. To better understand the evolution and diversity of these single-celled eukaryotes, we sequenced the genome of Ophryocystis elektroscirrha, a parasite of monarch butterflies, Danaus plexippus. The genome is miniscule, totaling only 9 million bases and containing fewer than 3,000 genes. We then compared this new sequence to the two other sequenced invertebrate-infecting apicomplexans, Porospora gigantea and Gregarina niphandrodes, which have nearly twice the gene content and found that O. elektroscirrha shares different orthologs with each sequenced relative, suggesting the true set of universally conserved apicomplexan genes is very small indeed. We investigated sequenced reads from other potential hosts to explore the viability of in silico infection screening. We recovered a similarly sized parasite genome from another butterfly, Danaus chrysippus, that was highly diverged from the O. elektroscirrha reference, possibly representing a distinct species. Using these two new genomes, we investigated potential evolutionary response by parasites to toxic phytochemicals their hosts ingest and sequester. Monarch butterflies are well-known to tolerate toxic cardenolides thanks to changes in the sequence of their Type II ATPase sodium pumps. We show that Ophryocystis completely lacks Type II or Type 4 sodium pumps, and related proteins PMCA calcium pumps show extreme sequence divergence compared to other Apicomplexa, demonstrating new avenues of research opened by genome sequencing of non-model Apicomplexa. Author SummaryThere are many relatives of Plasmodium, the single-celled parasites responsible for malaria, and they infect a wide range of animals, including insects. These parasites have received less attention however, leaving much unknown about them. We sequenced the genome of one such parasite, Ophryocystis elektroscirrha (OE), to compare it to better-studied parasites and shed light on OEs interaction with its host, the monarch butterfly. We found that OE has a tiny genome with the fewest genes of any sequenced parasite in this group, lacking many genes found in its relatives. Using our new data, we also discovered evidence that infections of other butterfly species that have been attributed to OE may be caused by a previously undiscovered distinct parasite species. And finally, we explored the evolution of a family of genes that may be targeted by medicinal plant compounds in the monarch butterflys diet; OE has lost one of these genes and radically changed the sequence of another, setting a direction for future research.

genomics↗

bioRxiv2019

Population genomics reveals complex patterns of immune gene evolution in monarch butterflies (Danaus plexippus)

Immune genes presumably rapidly evolve as pathogens exert strong selection pressures on host defense, but the evolution of immune genes is also constrained by trade-offs with other biological functions and shaped by the environmental context. Thus, immune genes may exhibit complex evolutionary patterns, particularly when organisms disperse to or live in variable environments. We examined the evolutionary patterns of the full set of known canonical immune genes within and among populations of monarch butterflies (Danaus plexippus), and relative to a closely related species (D. gilippus). Monarchs represent a system with a known evolutionary history, in which North American monarchs dispersed to form novel populations across the world, providing an opportunity to explore the evolution of immunity in the light of population expansion into novel environments. By analyzing a whole-genome resequencing dataset across populations, we found that immune genes as a whole do not exhibit consistent patterns of selection, differentiation, or genetic variation, but that patterns are specific to functional classes. Species comparisons between D. plexippus and D. gilippus and analyses of monarch populations both revealed consistently low levels of genetic variation in signaling genes, suggesting conservation of these genes over evolutionary time. Modulation genes showed the opposite pattern, with signatures of relaxed selection across populations. In contrast, recognition and effector genes exhibited less consistent patterns. When focusing on genes with exceptionally strong signatures of selection or differentiation, we also found population-specific patterns, consistent with the hypothesis that monarch populations do not face uniform selection pressures with respect to immune function.

evolutionary biology↗

bioRxiv2019

Transcriptomics of monarch butterflies (Danaus plexippus) reveals strong differential gene expression in response to host plant toxicity, but weak response to parasite infection

Herbivorous insects have evolved many mechanisms to overcome plant chemical defenses, including detoxification and sequestration. Herbivores may also use toxic plants to reduce parasite infection. Plant toxins could directly interfere with parasites or could enhance endogenous immunity. Alternatively, plant toxins could favor down-regulation of endogenous immunity by providing an alternative (exogenous) defense against parasitism. However, studies on genome-wide transcriptomic responses to plant defenses and the interplay between host plant toxicity and parasite infection remain rare. Monarch butterflies (Danaus plexippus) are specialist herbivores that feed on milkweeds (Asclepias spp.), which contain toxic cardenolides. Monarchs have adapted to cardenolides through multiple resistance mechanisms and can sequester cardenolides to defend against bird predators. In addition, high-cardenolide milkweeds confer medicinal effects to monarchs against a specialist protozoan parasite (Ophryocystis elektroscirrha). We used this system to study the interplay between the effects of plant toxicity and parasite infection on global gene expression. Our results demonstrate that monarch larvae differentially express several hundred genes when feeding on A. curassavica and A. incarnata, two species that are similar in nutritional content but differ substantially in cardenolide concentrations. These differentially expressed genes include genes within multiple families of canonical insect detoxification genes, suggesting that they play a role in monarch toxin resistance and sequestration. Interestingly, we found little transcriptional response to infection. However, parasite growth was reduced in monarchs reared on A. curassavica, and in these monarchs, a small number of immune genes were down-regulated, consistent with the hypothesis that medicinal plants can reduce reliance on endogenous immunity.

genomics↗

bioRxiv2018

Industrial bees: when agricultural intensification doesn’t impact local disease prevalence

O_LIAlthough it is generally thought that the intensification of farming will result in higher disease prevalences there is little specific modelling testing this idea. We build multi-colony models to inform how apicultural intensification is predicted to impact honeybee pathogen epidemiology at the apiary scale.\nC_LIO_LICounter to the prevailing view, our models predict that intensification, captured though increased population sizes, changes in population network structure, and increased between-colony transmission, is likely to have little effect on disease prevalence within an apiary.\nC_LIO_LIThe greatest impacts of intensification are found for diseases with relatively low R0 (basic reproduction number), however, such diseases cause little overall disease prevalence and therefore the impacts of intensification are minor. Furthermore, the smallest impacts of intensification are found for diseases with high R0 values, which we argue are typical of important honeybee diseases.\nC_LIO_LIPolicy Implications: Our findings highlight a lack of support for the hypothesis that current and ongoing intensification leads to notably higher disease prevalences. More broadly, our work demonstrates the need for informative models of agricultural systems and management practices in order to understand the implications of management changes on diseases.\nC_LI

epidemiology↗