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Evolutionary innovations have played an important role in shaping the diversity of life on Earth. However, how these innovations arise and their downstream effects on patterns of morphological diversification remain poorly understood. Here, we examine the impact of evolutionary innovation on trait diversification in tetraodontiform fishes (pufferfishes, boxfishes, ocean sunfishes, and allies). This order provides an ideal model system for studying morphological diversification owing to their range of habitats and divergent morphologies, including the fusion of the teeth into a beak in several families. Using three-dimensional geometric morphometric data for 176 extant and fossil species, we examine the effect of skull integration and novel habitat association on the evolution of innovation. Strong integration may be a requirement for rapid trait evolution and facilitating the evolution of innovative structures, like the tetraodontiform beak. Our results show that the beak arose in the presence of highly conserved patterns of integration across the skull, suggesting that integration did not limit the range of available phenotypes to tetraodontiforms. Furthermore, we find that beaks have allowed tetraodontiforms to diversify into novel ecological niches, irrespective of habitat. Our results suggest that general rules pertaining to evolutionary innovation may be more nuanced than previously thought.

 

Habitat transitions have shaped the evolutionary trajectory of many clades. Sea catfishes (Ariidae) have repeatedly undergone ecological transitions, including colonizing freshwaters from marine environments, leading to an adaptive radiation in Australia and New Guinea alongside non-radiating freshwater lineages elsewhere. Here, we generate and analyze one long-read reference genome and 66 short-read whole genome assemblies, in conjunction with genomic data for 54 additional species. We investigate how three major ecological transitions have shaped genomic variation among ariids over their ~ 50 million-year evolutionary history. Our results show that relatively younger freshwater lineages exhibit a higher incidence of positive selection than their more ancient marine counterparts. They also display a larger disparity in body shapes, a trend that correlates with a heightened occurrence of positive selection on genes associated with body size and elongation. Although positive selection in the Australia and New Guinea radiation does not stand out compared to non-radiating lineages overall, selection across the prolactin gene family during the marine-to-freshwater transition suggests that strong osmoregulatory adaptations may have facilitated their colonization and radiation. Our findings underscore the significant role of selection in shaping the genome and organismal traits in response to habitat shifts across macroevolutionary scales.

 

Migration independently evolved numerous times in animals, with a myriad of ecological and evolutionary implications. In fishes, perhaps the most extreme form of migration is diadromy, the migration between marine and freshwater environments. Key and long-standing questions are: how many times has diadromy evolved in fishes, how frequently do diadromous clades give rise to non-diadromous species, and does diadromy influence lineage diversification rates? Many diadromous fishes have large geographic ranges with constituent populations that use isolated freshwater habitats. This may limit gene flow between some populations, increasing the likelihood of speciation in diadromous lineages relative to nondiadromous lineages. Alternatively, diadromy may reduce lineage diversification rates if migration is associated with enhanced dispersal capacity that facilitates gene flow within and between populations. Clupeiformes (herrings, sardines, shads, and anchovies) is a model clade for testing hypotheses about the evolution of diadromy because it includes an exceptionally high proportion of diadromous species and several independent evolutionary origins of diadromy. However, relationships among major clupeiform lineages remain unresolved, and existing phylogenies sparsely sampled diadromous species, limiting the resolution of phylogenetically informed statistical analyses. We assembled a phylogenomic dataset and used multi-species coalescent and concatenation-based approaches to generate the most comprehensive, highly resolved clupeiform phylogeny to date, clarifying associations among several major clades and identifying recalcitrant relationships needing further examination. We determined that variation in rates of sequence evolution (heterotachy) and base-composition (nonstationarity) had little impact on our results. Using this phylogeny, we characterized evolutionary patterns of diadromy and tested for differences in lineage diversification rates between diadromous, marine, and freshwater lineages. We identified 13 transitions to diadromy, all during the Cenozoic Era (10 origins of anadromy, 2 origins of catadromy, and 1 origin of amphidromy), and 7 losses of diadromy. Two diadromous lineages rapidly generated nondiadromous species, demonstrating that diadromy is not an evolutionary dead end. We discovered considerably faster transition rates out of diadromy than to diadromy. The largest lineage diversification rate increase in Clupeiformes was associated with a transition to diadromy, but we uncovered little statistical support for categorically faster lineage diversification rates in diadromous versus nondiadromous fishes. We propose that diadromy may increase the potential for accelerated lineage diversification, particularly in species that migrate long distances. However, this potential may only be realized in certain biogeographic contexts, such as when diadromy allows access to ecosystems in which there is limited competition from incumbent species.

 

Almost nothing is known about the diets of bathypelagic fishes, but functional morphology can provide useful tools to infer ecology. Here we quantify variation in jaw and tooth morphologies across anglerfishes (Lophiiformes), a clade spanning shallow and deep-sea habitats. Deep-sea ceratioid anglerfishes are considered dietary generalists due to the necessity of opportunistic feeding in the food-limited bathypelagic zone. We found unexpected diversity in the trophic morphologies of ceratioid anglerfishes. Ceratioid jaws span a functional continuum ranging from species with numerous stout teeth, a relatively slow but forceful bite, and high jaw protrusibility at one end (characteristics shared with benthic anglerfishes) to species with long fang-like teeth, a fast but weak bite and low jaw protrusibility at the other end (including a unique ‘wolftrap’ phenotype). Our finding of high morphological diversity seems to be at odds with ecological generality, reminiscent of Liem's paradox (morphological specialization allowing organisms to have broader niches). Another possible explanation is that diverse ceratioid functional morphologies may yield similar trophic success (many-to-one mapping of morphology to diet), allowing diversity to arise through neutral evolutionary processes. Our results highlight that there are many ways to be a successful predator in the deep sea. 

Molecular studies have shown that Neotropical fishes of the order Characiformes have undergone two independent events of cave colonization. Among these fishes are the Mexican blind cavefish ( Astyanax mexicanus ), a well-studied model system for cave adaptation, and the lesser-known Brazilian blind characid ( Stygichthys typhlops ). Although various genomic and transcriptomic approaches have been used to identify genes responsible for cave adaptation in A. mexicanus , these genetic factors have not been explored in an evolutionary comparative framework in cave-adapted characiforms. To address this gap, we assembled a de novo transcriptome for the Brazilian blind characid, identifying 27,845 assembled unigenes, of which 22,580 were assigned as putative one-to-one orthologs to the Mexican cavefish. We then used the package RELAX to analyze 789 genes in cavefishes, identifying 311 genes under intensified or relaxed selection. Our analysis revealed 26 genes with signatures of convergent, relaxed selection linked to vision, circadian cycles, pigmentation, and hematopoiesis processes. Additionally, we conducted differential gene expression analyzes between the snout region and a control tissue sample (muscle), identifying 96 differentially expressed genes associated with cell-surface-bound and calcium-binding proteins. Our study offers insights into the genetic mechanisms underlying cave adaptation in characiform fishes, particularly the Brazilian blind characid. Moreover, our transcriptome dataset and list of genes under convergent, relaxed, and intensified selection serve as a valuable resource for future functional studies of genes involved in cave adaptation. Our work highlights the importance of examining genetic adaptations in multiple independent lineages to better understand the evolutionary processes underlying cave adaptation. 

Abstract High-risk human papillomaviruses (HPVs) 16 and 18 are responsible for more than 70% of cervical cancers and majority of other HPV-associated cancers world-wide. Current treatments for these cancers have limited efficacy, which in turn has resulted in disease recurrence and poor survival rates in advanced disease stages. Hence, there is a significant need for development of novel molecularly-targeted therapeutics. This can only be achieved through improved understanding of disease mechanism. Recently, we developed a Drosophila model of HPV18E6 plus human E3 ubiquitin ligase (hUBE3A) and demonstrated that the E6-induced cellular abnormalities are conserved between humans and flies. Subsequently, we demonstrated that reduced level and activity of IKKβ, a regulator of NF-κB, suppresses the cellular abnormalities induced by E6 oncoprotein and that the interaction of IKKβ and E6 is conserved in human cells. In this study, we performed transcriptomic analysis to identify differentially expressed genes that play a role in IKKβ-mediated suppression of E6-induced defects. Transcriptome analysis identified 215 genes whose expression was altered due to reduced levels of IKKβ. Of these 215 genes, 151 genes showed annotations. These analyses were followed by functional genetic interaction screen using RNAi, overexpression, and mutant fly strains for identified genes. The screen identified several genes including genes involved in Hippo and Toll pathways as well as junctional complexes whose downregulation or upregulation resulted in alterations of E6-induced defects. Subsequently, RT-PCR analysis was performed for validation of altered gene expression level for a few representative genes. Our results indicate an involvement for Hippo and Toll pathways in IKKβ-mediated suppression of E6 + hUBE3A-induced cellular abnormalities. Therefore, this study enhances our understanding of the mechanisms underlying HPV-induced cancer and can potentially lead to identification of novel drug targets for cancers associated with HPV. 

Body size is an important species trait, correlating with life span, fecundity, and other ecological factors. Over Earth’s geological history, climate shifts have occurred, potentially shaping body size evolution in many clades. General rules attempting to summarize body size evolution include Bergmann’s rule, which states that species reach larger sizes in cooler environments and smaller sizes in warmer environments, and Cope’s rule, which poses that lineages tend to increase in size over evolutionary time. Tetraodontiform fishes (including pufferfishes, boxfishes, and ocean sunfishes) provide an extraordinary clade to test these rules in ectotherms owing to their exemplary fossil record and the great disparity in body size observed among extant and fossil species. We examined Bergmann’s and Cope’s rules in this group by combining phylogenomic data (1,103 exon loci from 185 extant species) with 210 anatomical characters coded from both fossil and extant species. We aggregated data layers on paleoclimate and body size from the species examined, and inferred a set of time-calibrated phylogenies using tip-dating approaches for downstream comparative analyses of body size evolution by implementing models that incorporate paleoclimatic information. We found strong support for a temperature-driven model in which increasing body size over time is correlated with decreasing oceanic temperatures. On average, extant tetraodontiforms are two to three times larger than their fossil counterparts, which otherwise evolved during periods of warmer ocean temperatures. These results provide strong support for both Bergmann’s and Cope’s rules, trends that are less studied in marine fishes compared to terrestrial vertebrates and marine invertebrates. 

Repeatable, convergent outcomes are prima facie evidence for determinism in evolutionary processes. Among fishes, well-known examples include microevolutionary habitat transitions into the water column, where freshwater populations (e.g., sticklebacks, cichlids, and whitefishes) recurrently diverge toward slender-bodied pelagic forms and deep-bodied benthic forms. However, the consequences of such processes at deeper macroevolutionary scales in the marine environment are less clear. We applied a phylogenomics-based integrative, comparative approach to test hypotheses about the scope and strength of convergence in a marine fish clade with a worldwide distribution (snappers and fusiliers, family Lutjanidae) featuring multiple water-column transitions over the past 45 million years. We collected genome-wide exon data for 110 (∼80%) species in the group and aggregated data layers for body shape, habitat occupancy, geographic distribution, and paleontological and geological information. We also implemented approaches using genomic subsets to account for phylogenetic uncertainty in comparative analyses. Our results show independent incursions into the water column by ancestral benthic lineages in all major oceanic basins. These evolutionary transitions are persistently associated with convergent phenotypes, where deep-bodied benthic forms with truncate caudal fins repeatedly evolve into slender midwater species with furcate caudal fins. Lineage diversification and transition dynamics vary asymmetrically between habitats, with benthic lineages diversifying faster and colonizing midwater habitats more often than the reverse. Convergent ecological and functional phenotypes along the benthic–pelagic axis are pervasive among different lineages and across vastly different evolutionary scales, achieving predictable high-fitness solutions for similar environmental challenges, ultimately demonstrating strong determinism in fish body-shape evolution.