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Krabbenhoft, T. J.

Publications and source records attributed to Krabbenhoft, T. J..

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A Lake Charr Pangenome Reveals Highly Conserved Ohnologs as Drivers of Phenotypic Diversity

Whole-genome duplication (WGD) is hypothesized to spur evolutionary diversification by producing genome-wide duplicate gene sets (Ohnologs) that are initially functionally redundant but can diverge markedly as the effects of relaxed selection accumulate over time. However, the underlying mechanisms remain unclear, in part because genomic studies often reconstruct Ohnolog evolution over millions of years, during which subsequent mutations can obscure deep-time signals. Investigating the relationship between Ohnolog evolution and diversification on a contemporary timescale offers clearer insights. We explore this relationship in Lake Charr (Salvelinus namaycush), where [~]10% of genes are retained highly conserved polyploid duplicates following the Salmonid-Specific Fourth Round WGD. Using 31 chromosome-level assemblies of Lake Charr from morphologically and ecologically diverse populations, joined into a pangenome graph, we characterized 189,555 structural variants (SVs) that were significantly less likely to affect genes retained as sequence-conserved Ohnolog pairs, nuancing the hypothesis that gene redundancy, relaxed selection, and functional diversification are intertwined. However, we found that SVs affecting such conserved Ohnologs may be potent drivers of adaptive evolution. Notably, we identified a putative 938-Kb interchromosomal translocation containing 25 genes with highly conserved Ohnologs in a paralogous (but untranslocated) genomic block. This putative translocation appears to have facilitated Ohnolog divergence in ankrd11 and hp, genes putatively linked to craniofacial and lipid metabolic diversity in sympatric Lake Superior morphs. This research reveals that conserved Ohnologs previously presumed to be redundant remain a reservoir for adaptive change.

genomics↗

A genomic tool to tackle cryptic diversity demonstrates the potential for off-target use of GT-seq panels

A comprehensive understanding of life history is vital to successful species conservation and management. When different life history stages are accompanied by considerable morphological or cryptic variation, such as the egg and larval phases exhibited by most fishes, genomic tools are essential for identifying species so that early-life ecology questions can be studied. Genotyping-in-thousands by sequencing (GT-seq) has recently emerged as a targeted and efficient approach for species identification. We leveraged existing genomic and transcriptomic data to develop a GT-seq panel capable of differentiating the members of the Coregonus artedi complex, a radiation of salmonids in the Laurentian Great Lakes whose members are indistinguishable with mitochondrial DNA barcoding loci and are the focus of bi-national conservation initiatives. Our panel of 494 loci was able to assign fishes in the C. artedi complex to species and lake. We examined cross-amplification in other coregonines with overlapping distributions and found that congeneric Lake Whitefish (C. clupeaformis) cross-amplified at 94% of loci and confamilial Round and Pygmy Whitefish (Prosopium spp.) cross-amplified at 42% and 38% of loci, respectively. We adapted bioinformatic probes to account for Prosopium-specific variants including 22 new SNPs and developed a whitelist of 428 SNPs capable of distinguishing these whitefishes. Finally, we demonstrated performance by identifying 3,066 coregonine larvae and juveniles collected in spring 2019-2021 from Lake Superior. These results hold promise for future insights into the species-specific ecology of early life coregonines and demonstrate the flexibility of GT-seq panels, which may cross-amplify hundreds of informative genome-wide loci in related taxa.

genomics↗

Genomic Structural Variation Rescues a Classic Biological Invader from a Population Bottleneck

Invasion genetics presents a classic paradox: how do species successfully spread despite severe population bottlenecks? The brown treesnake (Boiga irregularis) in Guam represents a striking example of this phenomenon, having been introduced with only a handful of individuals. We show that the population endured an extreme bottleneck, with roughly half of the genome exhibiting runs of homozygosity, comparable to species of conservation concern. Despite this, we uncovered extensive diversity in the form of nearly 19,000 genomic structural variants, which affect almost eight times more of the genome than single-nucleotide variants and provide material for rescuing the population from inbreeding-driven declines. Structural variant density was highest in gene promoters, where recombination and DNA repair often occur, providing a mechanism for rapid evolution of gene-linked diversity. This diversity is enriched in genes vital for adaptive immunity and olfaction, suggesting genomic diversity in key chromosomal regions can rescue populations from inbreeding. This work has critical implications for invasion biology and conservation genetics practitioners. TEASERGenomic structural variants rescue a textbook biological invader from a population bottleneck and inbreeding

genomics↗

Microsynteny Analysis Clarifies the Early Diversification of Cypriniform Fishes

While genomic data are powerfully informative for phylogenetic inference, traditional sequence-based analyses can be confounded by issues like homoplasy and incomplete lineage sorting, leaving deep nodes unresolved. Synteny, the conservation of gene order along a chromosome, presents a promising alternative source of phylogenetic information that is potentially less prone to these issues. Here we compare sequence and synteny phylogenetic phylogenomic approaches to unravel the evolutionary history of Cypriniformes, one of the most species-rich lineages of freshwater fishes. This clade has been plagued by uncertainty, particularly concerning the phylogenetic relationships between its four major subclades: Gyrinocheilidae (algae eaters), Catostomidae (suckers), Cobitoidei (loaches), and Cyprinoidei (minnows and carps). Phylogenomic approaches require high-quality genomic resources, which have been lacking for the family Gyrinocheilidae, a key lineage for understanding cypriniform evolution. To address this, we generated the first chromosome-level genome assembly and annotation for the Chinese Algae Eater (Gyrinocheilus aymonieri). We utilized this new genome along with 42 other fish genomes to conduct comprehensive phylogenomic analyses and compare results from sequence-based methods with a microsynteny-based approach. Although chromosome-level macrosynteny is broadly conserved among cypriniforms, we demonstrate that microsynteny has impressive power to resolve deep phylogenetic nodes. Both sequence-based and microsynteny-based analyses find that Gyrinocheilidae is the sister lineage to all other cypriniforms, resolving a long-standing phylogenetic point of contention. However, while sequence-based analyses provided weak support for the relationships among the remaining subclades, our microsynteny analysis revealed a novel and strongly supported sister relationship between Catostomidae and Cyprinoidei. This conclusion is supported by a 3- to 12-fold greater number of shared microsynteny clusters (synapomorphies) compared to the alternative topologies. We also demonstrate that microsynteny synapomorphies often arise from gene family expansions. Conservation of synteny concentrated in specific genomic regions may harbor the genomic underpinnings of the unique aspects of these clades and have played an important role in the evolutionary history of these taxa. Together, these results provide a robust phylogenomic backbone for Cypriniformes. More broadly, our findings highlight the power of microsynteny to resolve recalcitrant phylogenetic nodes where sequence data is uninformative, while also underscoring the critical importance of high-quality reference genomes, as our work also shows that including fragmented assemblies can lead to spurious results. Beyond phylogenomics, our results also provide a functional genomics glimpse into how conserved, clade-specific blocks of collinear genes (synteny synapomorphies) might contribute to what makes this hyperdiverse clade so unique and evolutionarily successful.

evolutionary biology↗

The genome of the vining fern Lygodium microphyllum highlights genomic and functional differences between life phases of an invasive plant

Functional and genomic studies on the differences between gametophyte and sporophyte life phases remain scarce, yet unraveling these dynamics is crucial to understanding the biology of plants and the success of each phase under different environments. Here, we provide a novel reference genome for the highly invasive fern Lygodium microphyllum and compare the transcriptomic and epigenomic landscapes of the gametophyte and sporophyte life phases. We found differential regulation of developmental genes (homeobox and MADS-box clades) and usage of alternative isoforms that may play a role in the genomic determination of the haploid and diploid life stages. We further generated the first base pair-resolution methylome of a fern gametophyte, and determined that methylation patterns are remarkably similar between vegetative tissues despite their morphological and functional differences. By examining the physiological and transcriptomic responses of gametophytes and sporophytes to freezing stress, the most likely abiotic factor preventing further expansion of this invasive species, we show that life phases and tissues use alternative molecular pathways to respond to this stressor, underscoring the need to incorporate both life phases when developing effective mitigation strategies. These new genomic resources fill a gap in our understanding of fundamental plant biology and inform invasive species research. SIGNIFICANCEAll land plants undergo an alternation of generations between haploid gametophyte and diploid sporophyte life phases. How these disparate life phases are generated from a single genome, and the functional implications of these differences for plant success, is largely unknown. Moreover, understanding life-phase-specific differences in rapidly evolving populations, such as invasive species, is critical to developing effective management strategies. We assembled a chromosome-level genome and generated epigenomic and transcriptomic resources from gametophyte and sporophyte phases of the invasive fern Lygodium microphyllum, which is estimated to cost the U.S. more than $2 million annually. We highlight transcriptomic, epigenomic, and physiological variation between life phases and find support for the crucial role of the often overlooked gametophyte in the invasion process.

plant biology↗

Spotty distributions: Spotted Gar (Lepisosteus oculatus) and Spotted Sucker (Minytrema melanops) range expansion in eastern Lake Erie

Natural range expansions in warm-water freshwater fishes are currently not well understood, but shifts in native species distributions can be influenced by many factors, including habitat restoration or degradation and climate change. Here, we provide empirical evidence of range expansions observed in two native freshwater fish species in Lake Erie: the Spotted Gar (Lepisosteus oculatus) and Spotted Sucker (Minytrema melanops). We confirmed our field identifications of L. oculatus and M. melanops using mtDNA barcoding. Maximum likelihood phylogenetic analyses reveal that our samples confidently resolve in the L. oculatus and M. melanops clades respectively, with additional identification support from BLAST searches. Notably, we found no correlation between the increased detection rate of both species and an increase in sampling effort when compared to previous records. Historically, eastern Lake Erie experienced habitat degradation through channelization, siltation, dredging, and toxification of sediments. We hypothesize that recent habitat remediation efforts have provided suitable habitat for both species to recolonize shallow waters with densely vegetated habitat (>90% substrate coverage). Both species are likely to continue their northern expansion as habitats are restored and climatic changes favor warm-water fishes.

zoology↗

Lacustrine speciation associated with chromosomal inversion in a lineage of riverine fishes

Geographic isolation is the primary driver of speciation in many vertebrate lineages. This trend is exemplified by North American darters, a clade of freshwater fishes where nearly all sister species pairs are allopatric and separated by millions of years of divergence. One of the only exceptions is the Lake Waccamaw endemic Etheostoma perlongum and its riverine sister species E. maculaticeps, which have no physical barriers to gene flow. Here we show that lacustrine speciation of E. perlongum is characterized by morphological and ecological divergence likely facilitated by a large chromosomal inversion. While Etheostoma perlongum is phylogenetically nested within the geographically widespread E. maculaticeps, there is a sharp genetic and morphological break coinciding with the lake-river boundary in the Waccamaw River system. Despite recent divergence, an active hybrid zone, and ongoing gene flow, analyses using a de novo reference genome reveal a 9 Mb chromosomal inversion with elevated divergence between E. perlongum and E. maculaticeps. This region exhibits striking synteny with known inversion supergenes in two distantly related fish lineages, suggesting deep evolutionary convergence of genomic architecture. Our results illustrate that rapid, ecological speciation with gene flow is possible even in lineages where geographic isolation is the dominant mechanism of speciation.

evolutionary biology↗

Transcriptomic divergence predicts morphological and ecological variation underlying an adaptive radiation

Groups of sympatric taxa with low inter-specific genetic differentiation, but considerable ecological differences, offer great opportunities to study the dynamics of divergence and speciation. This is the case of ciscoes (Coregonus spp.) in the Laurentian Great Lakes, which are characterized by a complex evolutionary history and are commonly described as having undergone an adaptive radiation. In this study, morphometrics, stable isotopes and transcriptome sequencing were used to study the relationships within the Coregonus artedi complex in western Lake Superior. We observed general concordance for morphological, ecological and genomic variation, but the latter was more taxonomically informative as it showed less overlap among species in multivariate space. Low levels of genetic differentiation were observed between individuals morphologically identified as C. hoyi and C. zenithicus, and we hypothesize this could be associated with recent hybridization between the two species. Transcriptome-based single nucleotide polymorphisms exhibited significant divergence for genes associated with vision, development, metabolism and immunity, among species that occupy different habitats. This study highlights the importance of using an integrative approach when studying groups of taxa with a complex evolutionary history, as individual-level analyses of multiple independent datasets can provide a clearer picture of the patterns and processes associated with the origins of biodiversity.

evolutionary biology↗