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Daane, J. M.

Publications and source records attributed to Daane, J. M..

8 recordsLinked to original sources

Gene loss under constant cold reveals "natural knockout" loci in Antarctic notothenioid fishes

BackgroundGene loss is a major but often underappreciated mode of genome evolution. Genes loss can reflect relaxed selective constraint, neutral decay, compensation, or adaptive change; once fixed, however, they alter the inherited gene complement and can shape the evolutionary trajectories available to descendant lineages. Shared losses near the base of a radiation may therefore become part of the genomic background on which later specialization occurs. The Antarctic notothenioid (cryonotothenioid) radiation provides a powerful system for studying gene loss in an extreme polar environment: it diversified in the thermally stable Southern Ocean, and outgroups outside the clade allow ancestral gene presence to be inferred. ResultsUsing whole-genome alignments and orthology-aware comparative analyses across 11 cryonotothenioids and four non-Antarctic notothenioid outgroups, we systematically identified gene-inactivating mutations and reconstructed their phylogenetic distribution. After applying stringent filters to reduce reference bias, mitigate assembly and annotation artifacts, and exclude loci with detectable transcriptomic support, we identified 30 high-confidence single-copy orthologs with loss of coding potential across sampled cryonotothenioids but intact coding sequences in outgroups. These clade-wide losses affect genes associated with lipid and amino acid metabolism, water transport, renal glucose reabsorption, skeletal mineralization, circadian regulation, and tRNA modification pathways. We also identified 12 additional single-copy orthologs lost across examined icefishes but retained in red-blooded notothenioids and outgroups, including genes associated with oxygen transport, iron handling, erythroid biology, and vesicular trafficking. ConclusionsOur study provides a genome-wide catalog of coding-gene losses shared across sampled cryonotothenioids, together with additional lineage-specific losses in icefishes. Many of these losses occur in conserved genes associated with disease-relevant phenotypes in humans or model vertebrates, suggesting that Antarctic notothenioids offer a natural comparative system for studying how loss-of-function variants can persist in viable wild populations. These candidate natural knockouts provide testable hypotheses for how environmental buffering, paralog compensation, and pathway rewiring may shape vertebrate physiology under chronic cold.

genomics↗

Convergent reduction in skeletal density during benthic to pelagic transitions in Baikal sculpins

Habitat transitions are a major driver of morphological evolution. Teleost fishes have repeatedly transitioned from benthic to pelagic habitats, often evolving predictable changes in body shape that enhance hydrodynamic efficiency. While freshwater sculpins (Cottidae, Perciformes) are usually benthic, two genera in Lake Baikal, Comephorus and Cottocomephorus, have independently evolved into midwater niches. As sculpins lack a swim bladder, these lineages instead improved buoyancy through reduced skeletal density and increased lipid stores. Using micro-computed tomography and two-dimensional morphometrics, we characterized skeletal evolution across the Baikal sculpin radiation. We found that parallel changes in bone mineral density and microstructure independently evolved in the two pelagic clades. Density reductions occurred throughout the skull in pelagic species. The basibranchials and neurocranium exhibited the lowest overall bone density across all cranial elements. While the jaws maintained the highest absolute density values among the bones we measured, they also showed the greatest proportional reduction in density associated with pelagic habitat use, with a 56.86% decrease in percentage hydroxyapatite and a 21.39% increase in porosity. Morphometric analyses further identified convergence toward an elongate body shape, reduced and posteriorly shifted eyes, and elevated fin insertion in pelagic taxa. These results demonstrate a repeated skeletal lightening and body shape changes accompanying benthic-to-pelagic transitions. This pattern mirrors other benthic-to-pelagic transitions in teleosts that lack swim bladders, highlighting shared biomechanical and microstructural solutions to life in the open water.

evolutionary biology↗

Establishment, conservation, and innovation of dorsal determination mechanisms during the evolution of vertebrate paired appendages

Limb function requires polarized anatomy across the dorsal-ventral (DV) axis, but it is unclear when the capacity for DV differentiation of paired appendages arose in evolution. Here we define ancestral DV patterning programs in the fins of fishes. We show that the orthologue of the limb dorsal determinant, Lmx1b, is required to establish dorsality in zebrafish pectoral fins and is regulated by a conserved LARM cis-regulatory hub. However, lmx1bb expression in median fins is unaffected by removal of the LARM, suggesting its regulation is an evolutionary innovation specific to the paired appendages. Although we find the LARM is highly conserved across gnathostomes, we identify specific alteration of this region in hillstream loaches, fishes which naturally parallel "double-ventral" fin phenotypes observed in lmx1bb and LARM mutants. Altogether our findings indicate LARM-mediated dorsal identity is an ancestral feature of paired appendages that provide a prepattern for limb evolution and lineage diversification.

evolutionary biology↗

Convergent latitudinal erosion of circadian systems in a rapidly diversifying order of fishes

Biological clocks enable organisms to anticipate cyclical environmental changes. Some habitats, such as those at high latitudes or deep sea, experience seasonally diminished or absent diel cues upon which species entrain their circadian rhythms. Fishes of the order Perciformes have rapidly diversified and adapted to these arrhythmic ecosystems, raising the possibility that evolutionary modifications to their circadian biology contributes to their success as one of the most species-rich orders of vertebrates. Here, we used a comparative genomic approach to investigate patterns of biological clock gene loss and circadian rhythms across 33 perciform and six outgroup species. We found both widespread and lineage-specific loss and relaxed selection in core clock genes, particularly in the convergently evolving polar and deep-sea Notothenioidei and Cottioidei suborders. This trend of circadian gene loss was significantly correlated with latitude, with higher-latitude species showing greater loss. Whether these losses and relaxed selection lead to changes in circadian rhythms is unknown for most perciforms. To address this, we performed metabolic phenotyping on three notothenioid species and found no circadian metabolic oscillations during the late austral fall, including in the sub-Antarctic Eleginops maclovinus, sister to the Antarctic adaptive radiation. We propose that diminished reliance on endogenous biological clocks may be an adaptive feature that facilitates the survival and diversification of perciform fishes in polar and arrhythmic environments.

evolutionary biology↗

Phylogenomic analysis of the Lake Kronotskoe species flock of Dolly Varden charr reveals genetic signatures of sympatric radiation

Recent adaptive radiations provide evolutionary case studies, which provide the context to parse the relationship between genomic variation and the origins of distinct phenotypes. Sympatric radiations of the charr complex (genus Salvelinus) present a trove for phylogenetics as charrs have repeatedly diversified into multiple morphs with distinct feeding specializations. However, species flocks normally comprise only two to three lineages. Dolly Varden charr inhabiting Lake Kronotske represent the most extensive radiation described for the charr genus, containing at least seven lineages, each with defining morphological and ecological traits. Here, we perform the first genome-wide analysis of this species flock to parse the foundations of adaptive change. Our data support distinct, reproductively isolated lineages with little evidence of hybridization. We also find that specific selection on thyroid signaling and craniofacial genes forms a genomic basis for the radiation. Thyroid hormone is further implicated in subsequent lineage partitioning events. These results delineate a clear genetic basis for the diversification of specialized lineages, and highlight the role of developmental mechanisms in shaping the forms generated during adaptive radiation. Significance StatementDolly Varden Charr (Salvelinus malma) radiation in Lake Kronotskoe provides a unique case study of the genetics of adaptation and morphological evolution. We provide first genomic and experimental analyses of this radiation and show that major axes of change may be shaped by developmental constraints.

evolutionary biology↗

Refining Convergent Rate Analysis with Topology in Mammalian Longevity and Marine Transitions

The quest to map the genetic foundations of phenotypes has been empowered by the modern diversity, quality, and availability of genomic resources. Despite these expanding resources, the abundance of variation within lineages makes the association of genetic change to specific phenotypes improbable. Drawing such connections requires an a priori means of isolating the associated changes from background genomic variation. Evolution may provide these means via convergence; i.e., the shared variation that may result from replicate evolutionary experiments across independent trait occurrences. To leverage these opportunities, we developed TRACCER: Topologically Ranked Analysis of Convergence via Comparative Evolutionary Rates. As compared to current methods, this software empowers rate convergence analysis by factoring in topological relationships, because variation between phylogenetically proximate trait changes is more likely to be facilitating the trait. Pairwise comparisons are performed not with singular branches, but in reference to their most recent common ancestors. This ensures that comparisons represent identical genetic contexts and timeframes while obviating the problematic requirement of assigning ancestral states. We applied TRACCER to two case studies: marine mammal transitions, an unambiguous trait which has independently evolved three times, as well as the evolution of mammalian longevity, a less delineated trait but with more instances to compare. TRACCER, by factoring in topology, identifies highly significant, convergent genetic signals in these test cases, with important incongruities and statistical resolution when compared to existing convergence approaches. These improvements in sensitivity and specificity generate refined targets for downstream analysis of convergent evolution and identification of genotype-phenotype relationships.

genomics↗

Novel regulators of growth identified in the evolution of fin proportion in flying fish

Identifying the genetic foundations of trait variation and evolution is challenging as it is often difficult to parse meaningful signals from confounding signatures such as drift and epistasis. However, identification of the genetic loci underlying morphological and physiological traits can be honed through the use of comparative and complementary genetic approaches, whereby shared sets of genes that are repeatedly implicated across large evolutionary time periods as under selection can illuminate important pathways and epistatic relationships that function as novel regulators of trait development. Here we intersect comparative genomic analyses with unbiased mutagenesis screens in distantly related species to define the control of proportional growth, as changes in the size and relative proportions of tissues underlie a large degree of the variant forms seen in nature. Through a phylogenomic analysis of genome-wide variation in 35 species of flying fishes and relatives, we identify genetic signatures in both coding and regulatory regions underlying the convergent evolution of increased paired fin size and aerial gliding behaviors, key innovations for flying fishes and flying halfbeaks. To refine our analysis, we intersected convergent phylogenomic signatures with mutants identified in distantly related zebrafish with altered fin size. Through these paired approaches, we identify a surprising role for an L-type amino acid transporter, lat4a, and the potassium channel, kcnh2a, in the regulation of fin proportion. We show that specific epistatic interaction between these genetic loci in zebrafish closely phenocopies the observed fin proportions of flying fishes. The congruence of experimental and phylogenomic findings point to a conserved, non-canonical signaling interaction that integrates bioelectric cues and amino acid transport in the establishment of relative size in development and evolution.

developmental biology↗

Historical contingency shapes adaptive radiation in Antarctic fishes

Adaptive radiation illustrates the links between ecological opportunity, natural selection, and the generation of biodiversity (1). Central to adaptive radiation is the association between a diversifying lineage and the evolution of key traits that facilitate the utilization of novel environments or resources (2, 3). However, is not clear whether adaptive evolution or historical contingency is more important for the origin of key phenotypic traits in adaptive radiation (4, 5). Here we use targeted sequencing of >250,000 loci across 46 species to examine hypotheses concerning the origin and diversification of key traits in the adaptive radiation of Antarctic notothenioid fishes. Contrary to expectations of adaptive evolution, we show that notothenioids experienced a punctuated burst of genomic diversification and evolved key skeletal modifications before the onset of polar conditions in the Southern Ocean. We show that diversifying selection in pathways associated with human skeletal dysplasias facilitates ecologically important variation in buoyancy among Antarctic notothenioid species, and demonstrate the sufficiency of altered trip11, col1a2 and col1a1 function in zebrafish (Danio rerio) to phenocopy skeletal reduction in Antarctic notothenioids. Rather than adaptation being driven by the cooling of the Antarctic (6), our results highlight the role of exaptation and historical contingency in shaping the adaptive radiation of notothenioids. Understanding the historical and environmental context for the origin of key traits in adaptive radiations provides context in forecasting the effects of climate change on the stability and evolvability of natural populations.

evolutionary biology↗