Paul B. Frandsen’s research while affiliated with Brigham Young University - Provo Main Campus and other places

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Publications (132)


Figure 4: Composition of "Pondwatch" Observations 268
List of COI primers used in this study, including modified sequences containing 177 degenerate bases, accounting for variation in the target sequence. 178
Environmental DNA vs. Community Science: Strengths and Limitations for Urban Odonata Surveys
  • Preprint
  • File available

November 2024

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2 Reads

Rhema Uche-Dike

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Christian Benischek

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The study of insect decline remains a major frontier in the study of insect biodiversity and conservation. Despite growing concern about the decline rates of insects generally, relatively little data has been compiled about species of aquatic insects. Data is particularly lacking on the distribution of aquatic insects in urban ecosystems. Here, we compare environmental DNA (eDNA) metabarcoding and community science observation as means of monitoring Odonata in an urban habitat in Southwest Idaho. We show that the distribution of Odonata across this urban landscape is not uniform and that both monitoring methods have different strengths and weaknesses. We found that eDNA metabarcoding was very sensitive to the identification of genera from underrepresented families in the region, but was unable to distinguish between closely related genera, particularly from localities where eDNA could accumulate more data. On the other hand, community science observations effectively identified the presence of genera from more speciose families but missed the presence of relatively rare species, and those that had a short flight season. These findings suggest that eDNA and community science are highly complementary of each other, but if only one method is going to be used for a monitoring or conservation project, care should be given to account for the biases of each approach.

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Figure 1: Population Genomics of Kapokapowai 326
Figure 3: Niche Models of Kapokapowai Populations 448
Fst values between putative species of Kapokapowai
Elevational and Oceanic Barriers Shape the Distribution, Dispersal and Diversity of Aotearoa's Kapokapowai (Uropetala) Dragonflies

November 2024

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19 Reads

Mountains and islands are both model systems for studying the biogeography of diversification and population fragmentation. Aotearoa is an excellent location to study both phenomena due to alpine emergence and oceanic separation. While it would be expected that separation across Te Moana o Raukawa and elevation gradients are major barriers to gene flow in aquatic insects, such hypotheses have not been thoroughly explored in these taxa. Here, we show that mountains and oceanic separation function as semi-permeable barriers for Kapokapowai dragonflies. We show that, although Te Moana o Raukawa, is likely responsible for some of the genetic structure observed, speciation has not yet occurred in populations separated by the strait. Although there is no evidence that they are an impervious barrier, Kā Tiritiri-o-te-Moana do represent a major barrier to gene flow between named species. The distribution of alpine Kapokapowai can also not be explained by the ancestral populations simply rising with the uplifted tectonic plates. Although further research is needed, our findings suggest that the ancestral Kapokapowai colonized alpine habitats after their formation, and then radiated back out to lowlands. These findings suggest that aquatic insects could be an exciting new frontier in the study of the biogeography of Aotearoa.


Influence of water source on alpine stream community structure: linking morphological and metabarcoding approaches

November 2024

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26 Reads

Aquatic Sciences

Alpine streams support unique biodiversity because of their isolation in the river network and harsh environmental conditions. Variation in water sources to alpine streams are an important driver of benthic community structure; however, studies with long-term data on stream abiotic characteristics and biological communities remain relatively rare. This is especially true for very high elevations where effects of climate change will be most pronounced. We used a combination of morphological and metabarcoding approaches to characterize benthic communities at nine locations within a high elevation catchment (~ 3200 to 3700 m) in the Southern Rocky Mountains, USA. Survey sites included ephemeral and permanent streams dominated by glacier meltwater, snowmelt, lake outflows, and mixed-source waters. Discharge, water temperature, conductivity, pH, total dissolved nitrogen, and total dissolved phosphorus differed between water source types. Environmental differences between source water types reflected their position in the catchment, the influence of subsurface ice meltwater on nitrogen and ions, and the biological activity and stabilizing effects of lakes. In total, we detected 130 macroinvertebrate taxa (52 via morphology and 99 via metabarcoding). Macroinvertebrate composition was more strongly correlated with stream permanence and conductivity than with water temperature or nutrient availability. Glacial and snowmelt-fed streams were dominated by Chironomidae (especially Diamesinae) and Oligochaeta, with increasing richness of Plecoptera, Ephemeroptera, and Trichoptera at the lake-outlet and mixed-source sites. Lake outlets showed the highest beta diversity, with unique communities dominated by various filter feeders (Simuliidae and Sphaeriidae). Alpha diversity was similar at the glacial, snowmelt, and lake outlet sites, but increased at the downstream mixed-source sites which had proportionally more non-dipteran taxa. Our results support the idea that distinct source waters have unique environmental conditions, leading to variation in their community structure. These results provide motivation for conservation efforts that protect a diversity of alpine stream types within and between catchments.


Whole-genome assembly and annotation of the firecracker penstemon ( Penstemon eatonii )

October 2024

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14 Reads

Journal of Heredity

The penstemons are ornamental annual flowering plants native to the Intermountain West and Rocky Mountains and commonly used for urban landscaping. Elite commercial penstemons are generally susceptible to abiotic stresses, including drought, root rot, cold, and high salinity. Firecracker penstemon (Penstemon eatonii), however, is much more tolerant to these stresses than most elite cultivars. Importantly, firecracker penstemon has been reported to hybridize with many other penstemons and therefore provides the opportunity to develop more tolerant elite cultivars through strategic crossing. To facilitate the study and utilization of firecracker penstemon, we sequenced and annotated the genome of a P. eatonii accession collected from Utah, USA. We also performed low-coverage, whole-genome sequencing of 26 additional accessions from three different varieties of P. eatonii. This chromosome-scale genome assembly is the most contiguous and complete Penstemon genome sequenced to date.


(a) Male habitus of Druceiella hillmani (Hepialidae), this specimen was sampled to construct the genome in the present study (b) Dorsal (right) and ventral (left) views of male tergum VIII and genitalia (left) of the sequenced sample.
Comparison of genome sizes in 548 species of Lepidoptera. Genome assemblies for this analysis were chosen based on a BUSCO completeness >80% and duplication rate <5%. Box plots represent the mean genome size across 21 superfamilies within Lepidoptera. The genome of Druceiella hillmani (second from left) was among the largest of the 548 available high-quality Lepidoptera genomes that were compared.
Gene map of coding gene blast results against the RefSeq non-redundant (nr) protein database from NCBI. The best hit (defined by lowest e-value) was selected for each gene, and the order of the corresponding species was mapped to the contigs. Most genes had their best blast hit to lepidopteran species, and no contig was found to harbor genes dominantly from a different order than Lepidoptera.
A near chromosome-level genome assembly of a ghost moth (Lepidoptera, Hepialidae)

October 2024

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87 Reads

Scientific Data

Ghost moths are an unusual family of primitive moths (Lepidoptera: Hepialidae) known for their large body size and crepuscular adult activity. These moths represent an ancient lineage, frequently have soil dwelling larvae, and are adapted to high elevations, deserts, and other extreme environments. Despite being rather speciose with more than 700 species, there is a dearth of genomic resources for the family. Here, we present the first high quality, publicly available hepialid genome, generated from an Andean species of ghost moth, Druceiella hillmani. Our genome assembly has a length of 2,586 Mbp with contig N50 of 28.1 Mb and N50 of 29, and BUSCO completeness of 97.1%, making it one of the largest genomes in the order Lepidoptera. Our assembly is a vital resource for future research on ghost moth genomics.


Environment and diet shape the geography-specific Drosophila melanogaster microbiota composition

October 2024

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8 Reads

Geographic and environmental variation in the animal microbiota can be directly linked to the evolution and wild fitness of their hosts but often appears to be disordered. Here, we sought to better understand patterns that underlie wild variation in the microbiota composition of Drosophila melanogaster . First, environmental temperature predicted geographic variation in fly microbial communities better than latitude did. The microbiota also differed between wild flies and their diets, supporting previous conclusions that the fly microbiota is not merely a reflection of diet. Flies feeding on different diets varied significantly in their microbiota composition, and flies sampled from individual apples were exceptionally depauperate for the Lactic Acid Bacteria (LAB), a major bacterial group in wild and laboratory flies. However, flies bore significantly more LAB when sampled from other fruits or compost piles. Follow-up analyses revealed that LAB abundance in the flies uniquely responds to fruit decomposition, whereas other microbiota members better indicate temporal seasonal progression. Finally, we show that diet-dependent variation in the fly microbiota is associated with phenotypic differentiation of fly lines collected in a single orchard. These last findings link covariation between the flies’ dietary history, microbiota composition, and genetic variation across relatively small (single-orchard) landscapes, reinforcing the critical role that environment-dependent variation in microbiota composition can play in local adaptation and genomic differentiation of a model animal host. SIGNIFICANCE STATEMENT The microbial communities of animals influence their hosts’ evolution and wild fitness, but it is hard to predict and explain how the microbiota varies in wild animals. Here, we describe that the microbiota composition of wild Drosophila melanogaster can be ordered by temperature, humidity, geographic distance, diet decomposition, and diet type. We show how these determinants of microbiota variation can help explain lactic acid bacteria (LAB) abundance in the flies, including the rarity of LAB in some previous studies. Finally, we show that wild fly phenotypes segregate with the flies’ diet and microbiota composition, illuminating links between the microbiota and host evolution. Together, these findings help explain how variation in microbiota compositions can shape an animal’s life history.


Fig. 2. Reference genome assembly and genomic sequencing of C. ruber reveals two genetically distinct populations with unique demographic histories. a) Circos plot of the RagTag reference genome assembly displaying gene density, repeat content, CG content, and toxin gene families mapped to chromosome scaffolds as represented by corresponding colored lines. Toxin families are (ordered by chromosome): KUN, Kunitz-type toxin; CRISP, cytesine-rich secretory protein; NUC, nucleotidase; PDE, phosphodiesterase; VEGF, vascular endothelial growth factor; MYO, myotoxin; 3FTx, three-finger toxin; NGF, nerve growth factor; BPP, bradykinin-potentiating peptide; HYAL, hyaluronidase; CTL, C-type lectin; SVMP, snake venom metalloproteinase; SVSP, snake venom serine proteinase; PLA 2 , phospholipase A 2 . b-c) Population structure characterized from short-read WGS and ddRADseq data using ConStruct spatial models with b) K = 2 and c) K = 3. Maps depict individuals as pie charts reflecting ancestry proportions contributed by each genetic cluster. d) Estimated effective migration surface from WGS and ddRADseq data using EEMS. Shading indicates areas with relatively high (orange) and low (blue) landscape resistance to gene flow compared to a null area-wide model of isolation-by-distance (IBD). Plotted values of log(m) are effective migration rates relative to the overall migration rate across the study area. Circles represent sampling locations, and circle size corresponds to sampling density. e) Estimates of demographic histories across the two distinct populations from panel (b). Lines represent effective population size (N e ) estimated from eight individuals using a generation length of 3.3 years and a mutation rate of 0.007 per lineage per million years. Colors indicate N e estimates of individuals sampled from the northern population (warm) and southern population (cool; as determined in panel (b)). Contact zone (∼ 26 • N) is indicated throughout.
Fig. 3. Differential venom expression across life history and geographic space in C. ruber. a) Principal Component Analysis of venom-gland transcriptome DESEQ2 normalized count data, and b) Regression of Principal Component 1 (PC1) with SVL. Dotted line at 65 cm SVL shows the cut-off used for age class designation. Proportion of variance accounted for in PC1 and PC2 was 31% and 13%, respectively. c-d) Volcano plots of differential expression calculated from DESeq2 between populations c) and age classes d). Vertical dotted lines represent LFC ≥ 1, and horizontal dotted line represents α ≤ 0.05. Green points in each plot denote significantly DE toxin transcripts, and their placement denotes group bias. SVL, snout-vent-length; BPP, bradykinin-potentiating peptide; CRISP, cytesine-rich secretory protein; CTL, C-type lectin; MYO, myotoxin; PLA 2 , phospholipase A 2 ; SVMP, snake venom metalloproteinase; SVSP, snake venom serine proteinase.
Genome assembly statistics for C. ruber
Results of the conditional RDA for venom-gland transcriptome normalized read count data from HTSeq-count as the response variable
Significant variables of the marginal models identified through forward model selection from conditional RDAs using the top six most abundantly expressed toxin families
Where the “ ruber ” Meets the Road: Using the Genome of the Red Diamond Rattlesnake to Unravel the Evolutionary Processes Driving Venom Evolution

September 2024

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142 Reads

Genome Biology and Evolution

Understanding the proximate and ultimate causes of phenotypic variation is fundamental in evolutionary research, as such variation provides the substrate for selection to act upon. Although trait variation can arise due to selection, the importance of neutral processes is sometimes understudied. We presented the first reference-quality genome of the Red Diamond Rattlesnake (Crotalus ruber) and used range-wide ‘omic data to estimate the degree to which neutral and adaptive evolutionary processes shaped venom evolution. We characterized population structure and found substantial genetic differentiation across two populations, each with distinct demographic histories. We identified significant differentiation in venom expression across age classes with substantially reduced but discernible differentiation across populations. We then used conditional redundancy analysis to test whether venom expression variation was best predicted by neutral divergence patterns or geographically-variable (a)biotic factors. Snake size was the most significant predictor of venom variation, with environment, prey availability, and neutral sequence variation also identified as significant factors, though to a lesser degree. By directly including neutrality in the model, our results confidently highlight the predominant, yet not singular, role of life history in shaping venom evolution.


Figure 2 | Associations between temperature, pressure, and type III antifreeze protein copy number. 254 Relationships between AFP III copy number and (A) thermal minima of species habitats and (B) mean 255 pressure of species' habitats are plotted. Fitted lines represent fit from a phylogenetically controlled model 256 of type III antifreeze protein copy number. 257 258
Figure 4 | Effects of thermal minimum and pressure on copy number of syntenicically-conserved and 351 translocated type III antifreeze protein genes. Densities represent the posterior probabilities for fixed effects 352 (!) of (A) thermal minimum and (B) mean pressure on antifreeze protein copy in ancestral, syntenically-353 conserved versus translocated sites. 354 355 356 Molecular repair mechanisms causing variation in copy number such as break-induced
Temperature and Pressure Shaped the Evolution of Antifreeze Proteins in Polar and Deep Sea Zoarcoid Fishes

August 2024

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43 Reads

Antifreeze proteins (AFPs) have enabled teleost fishes to repeatedly colonize polar seas. Four AFP types have convergently evolved in several fish lineages. AFPs inhibit ice crystal growth and lower cellular freezing point. In lineages with AFPs, species inhabiting colder environments may possess more AFP copies. Elucidating how interspecific differences in AFP copy number evolve is challenging due to the genes' tandem array structure and consequently poor resolution of these repetitive regions. Here we explore the evolution of type III AFPs (AFP III) in the globally distributed suborder Zoarcoidei, leveraging six new long-read genome assemblies. Zoarcoidei has fewer genomic resources relative to other polar fish clades while it is one of the few groups of fishes adapted to both the Arctic and Southern Oceans. Combining these new assemblies with additional long-read genomes available for Zoarcoidei, we conducted a comprehensive phylogenetic test of AFP III evolution and modeled the effects of thermal habitat and depth on AFP III gene family evolution. We confirm a single origin of AFP III via neofunctionalization of the enzyme sialic acid synthase B and show that AFP gains and losses were not only correlated with temperature, but also with depth, which reduces freezing via pressure. Associations between the environment and AFP III copy number were driven by duplications of paralogs that were translocated out of the ancestral locus at which Zoarcoidei AFP arose. Our results reveal novel environmental effects on AFP evolution and demonstrate the value of high-quality genomic resources for studying how structural genomic variation shapes convergent adaptation.


Evolution of Opsin Genes in Caddisflies (Insecta: Trichoptera)

August 2024

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46 Reads

Genome Biology and Evolution

Insects have evolved complex and diverse visual systems in which light-sensing protein molecules called “opsins” couple with a chromophore to form photopigments. Insect photopigments group into three major gene families based on wavelength sensitivity: long wavelength (LW), short wavelength (SW), and ultraviolet wavelength (UV). In this study, we identified 123 opsin sequences from whole-genome assemblies across 25 caddisfly species (Insecta: Trichoptera). We discovered the LW opsins have the most diversity across species and form two separate clades in the opsin gene tree. Conversely, we observed a loss of the SW opsin in half of the trichopteran species in this study, which might be associated with the fact that caddisflies are active during low-light conditions. Lastly, we found a single copy of the UV opsin in all the species in this study, with one exception: Athripsodes cinereus has two copies of the UV opsin and resides within a clade of caddisflies with colorful wing patterns.


Figure 2. Kmer histogram and Hi-C contact map. (A) Genomescope Profile of kmers derived from HiFi reads. (B) Hi-C contact map of the 14 chromosome-length scaffolds,
Current stonefly genome assemblies and quality statistics as of 2024
An unusually large genome from an unusually large stonefly: A chromosome-length genome assembly for the giant salmonfly, Pteronarcys californica (Plecoptera: Pteronarcyidae)

August 2024

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111 Reads

Journal of Heredity

Pteronarcys californica (Newport 1848) is commonly referred to as the giant salmonfly and is the largest species of stonefly (Insecta: Plecoptera) in the western United States. Historically, it was widespread and abundant in western rivers, but populations have experienced a substantial decline in the past few decades, becoming locally extirpated in numerous rivers in Utah, Colorado, and Montana. Although previous research has explored the ecological variables conducive to the survivability of populations of the giant salmonfly, a lack of genomic resources hampers exploration of how genetic variation is spread across extant populations. To accelerate research on this imperiled species, we present a de novo chromosomal-length genome assembly of P. californica generated from PacBio HiFi sequencing and Hi-C chromosome conformation capture. Our assembly includes 14 predicted pseudo chromosomes and 98.8% of Insecta universal core orthologs. At 2.40 gigabases, the P. californica assembly is the largest of available stonefly assemblies, highlighting at least 9.5-fold variation in assembly size across the order. Repetitive elements (REs) account for much of the genome size increase in P. californica relative to other stonefly species, with the content of Class I retroelements alone exceeding the entire assembly size of all but two other species studied. We also observed preliminary suborder-specific trends in genome size that merit testing with more robust taxon sampling.


Citations (56)


... A new perspective on the phylogeny of caddisflies is provided by a recent paper by Frandsen et al. [9]. That paper incorporates new transcriptomes, targeted exon capture and publicly available genomes, resulting in a dataset that represents 207 trichopteran species, 174 genera and 48 of 52 extant families. ...

Reference:

Evolutionary story of caddisflies: new insights from phylogenomics
Phylogenomics recovers multiple origins of portable case making in caddisflies (Insecta: Trichoptera), nature’s underwater architects

... All extant higher groups within the order, however, began to diversify in the Triassic, including Annulipalpia (fixed retreat makers), Hydroptiloidea (purse case makers), Rhyacophiloidea (free-living and tortoise case makers) and Phryganides (tube case makers) (electronic supplementary material, table S7). Notably, tube-case-making caddisflies within the infraorder Plenitentoria, the group that includes multiple lineages that construct their cases from flowering plant matter, originated in the mid-Jurassic approximately 170 million years ago [30]. ...

Revised chronology of Trichoptera evolution

Contributions to Entomology

... Following gene prediction in GALBA, we used blastP 2.9.0+ (NCBI 2019) with a filter of 1e-25 to identify annotated genes that had orthologues in the annotated protein sets of the polyneopteran species Bacillus rossius (Lavanchy et al. 2024), Dryococelus australis (Stuart et al. 2024), Coptotermes formosanus (Itakura et al. 2020), Diploptera punctata (Fouks et al. 2023), Periplaneta americana (Li et al. 2018), Schistocerca americana (Childers et al. 2021), Schistocerca gregaria (Verlinden et al. 2020), and Timema podura (Comeault et al. 2016). This filtering approach has previously been shown to increase the specificity of GALBA annotations by removing spurious gene annotations, with a minimal reduction of sensitivity (Tolman et al. 2023). We evaluated the completeness of the annotation with the insecta_odb10 dataset with BUSCO 4.1.4 ...

Newly Sequenced Genomes Reveal Patterns of Gene Family Expansion in Select Dragonflies (Odonata: Anisoptera)

... To expand our taxon sampling to include museum specimens, we used anchored hybrid enrichment (AHE) [28,29]. We used a probe set previously used by Pauls et al. [40]. Using this method, we identified approximately 900 exons suitable for phylogenetic inference (electronic supplementary material, §3). ...

Gill Structure Linked to Ecological and Species Diversification in a Clade of Caddisflies

Arthropod Systematics and Phylogeny

... Genome assembly and quality assessment. We assembled the genome using our previously published genome-assembly pipeline 9,10 . Briefly, raw HiFi ccs reads were fed to the Hifiasm assembler, and the assembled output was purged for duplicated haplotigs using purge_haplotigs v1.1.2 ...

New genome reveals molecular signatures of adaptation to nocturnality in moth-like butterflies (Hedylidae)

... A new genus and species of dragonflies (Odonata, Zygoptera) were discovered from the USA (Archibald, S.B., & Cannings, R. A., 2021). 250 million years ago, dragonflies and butterflies developed separately, and their current status was studied at the molecular genetic level in the scientific data of E. R. Tolman et al. (2023) (Tolman, E. R., et al., 2023) Ischnura elegans and Platycnemis pennipes, and two dragonfly species, Pantala flavescens and Tanypteryx hageni, we demonstrate that the autosomes of Odonata have undergone few fission, fusion, or inversion events, despite 250 million years of separation. In the four genomes discussed here, our results show that all autosomes have a clear ortholog in the ancestral karyotype. ...

Exploring chromosome evolution in 250 million year old groups of dragonflies and damselflies (Insecta:Odonata)

Molecular Ecology

... The third example showed that repetitive sequences may contribute to false analyses in genome editing, making it difficult to distinguish between actual targeted sequences and similar sequences found elsewhere in the genome. We note that repetitive sequences are ubiquitous features in many genomes [18,43], with some non-model arthropod species harboring remarkably high levels compared to the model organisms [44]. The above three representative examples underscore the importance of taking the genetic background of the target regions into consideration when interpreting CRISPR/Cas editing results in any organism. ...

600+ insect genomes reveal repetitive element dynamics and highlight biodiversity-scale repeat annotation challenges
  • Citing Article
  • September 2023

Genome Research

... Recent genome sequencing has demonstrated homology between several bH and bL genes in terrestrial moths and aquatic caddis ies [11][12][13][14] . The bH gene is large, has short, conserved characteristic sequences at both ends, and variable repetitive sequences in its central region. ...

Characterization of the primary structure of the major silk gene, h-fibroin, across caddisfly (Trichoptera) suborders

iScience

... Dried museum specimens and outgroups showed the greatest levels of missing data and recovered variably long branches in phylogenetic reconstructions (Figures 2, S2-S11, Table S2). Such effects associated with target capture studies using older museum specimens are known in insects and other arthropods (Blaimer et al., 2016;Freitas et al., 2023;Goodman et al., 2023) and are especially well documented in birds (Decicco et al., 2023;Hruska et al., 2023;Lim & Braun, 2016;Moyle et al., 2016;Ostrow et al., 2023;Salter et al., 2022). It is likely that processing captured data outside of Phyluce (e.g. ...

Assessment of targeted enrichment locus capture across time and museums using odonate specimens

Insect Systematics and Diversity