Landscape dynamics and diversification of the megadiverse South American freshwater fish fauna.

Landscape dynamics are widely thought to govern the tempo and mode of continental radiations, yet the effects of river network rearrangements on dispersal and lineage diversification remain poorly understood. We integrated an unprecedented occurrence dataset of 4,967 species with a newly compiled, time-calibrated phylogeny of South American freshwater fishes-the most species-rich continental vertebrate fauna on Earth-to track the evolutionary processes associated with hydrogeographic events over 100 Ma. Net lineage diversification was heterogeneous through time, across space, and among clades. Five abrupt shifts in net diversification rates occurred during the Paleogene and Miocene (between 30 and 7 Ma) in association with major landscape evolution events. Net diversification accelerated from the Miocene to the Recent (c. 20 to 0 Ma), with Western Amazonia having the highest rates of in situ diversification, which led to it being an important source of species dispersing to other regions. All regional biotic interchanges were associated with documented hydrogeographic events and the formation of biogeographic corridors, including the Early Miocene (c. 23 to 16 Ma) uplift of the Serra do Mar and Serra da Mantiqueira and the Late Miocene (c. 10 Ma) uplift of the Northern Andes and associated formation of the modern transcontinental Amazon River. The combination of high diversification rates and extensive biotic interchange associated with Western Amazonia yielded its extraordinary contemporary richness and phylogenetic endemism. Our results support the hypothesis that landscape dynamics, which shaped the history of drainage basin connections, strongly affected the assembly and diversification of basin-wide fish faunas.

Squalomix: shark and ray genome analysis consortium and its data sharing platform.

The taxon Elasmobranchii (sharks and rays) contains one of the long-established evolutionary lineages of vertebrates with a tantalizing collection of species occupying critical aquatic habitats. To overcome the current limitation in molecular resources, we launched the Squalomix Consortium in 2020 to promote a genome-wide array of molecular approaches, specifically targeting shark and ray species. Among the various bottlenecks in working with elasmobranchs are their elusiveness and low fecundity as well as the large and highly repetitive genomes. Their peculiar body fluid composition has also hindered the establishment of methods to perform routine cell culturing required for their karyotyping. In the Squalomix consortium, these obstacles are expected to be solved through a combination of in-house cytological techniques including karyotyping of cultured cells, chromatin preparation for Hi-C data acquisition, and high fidelity long-read sequencing. The resources and products obtained in this consortium, including genome and transcriptome sequences, a genome browser powered by JBrowse2 to visualize sequence alignments, and comprehensive matrices of gene expression profiles for selected species are accessible through https://github.com/Squalomix/info.

Adaptive shifts underlie the divergence in wing morphology in bombycoid moths.

The evolution of flapping flight is linked to the prolific success of insects. Across Insecta, wing morphology diversified, strongly impacting aerodynamic performance. In the presence of ecological opportunity, discrete adaptive shifts and early bursts are two processes hypothesized to give rise to exceptional morphological diversification. Here, we use the sister-families Sphingidae and Saturniidae to answer how the evolution of aerodynamically important traits is linked to clade divergence and through what process(es) these traits evolve. Many agile Sphingidae evolved hover feeding behaviours, while adult Saturniidae lack functional mouth parts and rely on a fixed energy budget as adults. We find that Sphingidae underwent an adaptive shift in wing morphology coincident with life history and behaviour divergence, evolving small high aspect ratio wings advantageous for power reduction that can be moved at high frequencies, beneficial for flight control. By contrast, Saturniidae, which do not feed as adults, evolved large wings and morphology which surprisingly does not reduce aerodynamic power, but could contribute to their erratic flight behaviour, aiding in predator avoidance. We suggest that after the evolution of flapping flight, diversification of wing morphology can be potentiated by adaptative shifts, shaping the diversity of wing morphology across insects.

The whale shark genome reveals patterns of vertebrate gene family evolution.

Chondrichthyes (cartilaginous fishes) are fundamental for understanding vertebrate evolution, yet their genomes are understudied. We report long-read sequencing of the whale shark genome to generate the best gapless chondrichthyan genome assembly yet with higher contig contiguity than all other cartilaginous fish genomes, and studied vertebrate genomic evolution of ancestral gene families, immunity, and gigantism. We found a major increase in gene families at the origin of gnathostomes (jawed vertebrates) independent of their genome duplication. We studied vertebrate pathogen recognition receptors (PRRs), which are key in initiating innate immune defense, and found diverse patterns of gene family evolution, demonstrating that adaptive immunity in gnathostomes did not fully displace germline-encoded PRR innovation. We also discovered a new toll-like receptor (TLR29) and three NOD1 copies in the whale shark. We found chondrichthyan and giant vertebrate genomes had decreased substitution rates compared to other vertebrates, but gene family expansion rates varied among vertebrate giants, suggesting substitution and expansion rates of gene families are decoupled in vertebrate genomes. Finally, we found gene families that shifted in expansion rate in vertebrate giants were enriched for human cancer-related genes, consistent with gigantism requiring adaptations to suppress cancer.

Chromosome-Level Genome Assembly of Chinese Sucker (Myxocyprinus asiaticus) Reveals Strongly Conserved Synteny Following a Catostomid-Specific Whole-Genome Duplication.

Fishes of the family Catostomidae ("suckers"; Teleostei: Cypriniformes) are hypothesized to have undergone an allopolyploidy event approximately 60 Ma. However, genomic evidence has previously been unavailable to assess this hypothesis. We sequenced and assembled the first chromosome-level catostomid genome, Chinese sucker (Myxocyprinus asiaticus), and present clear evidence of a catostomid-specific whole-genome duplication (WGD) event ("Cat-4R"). Our results reveal remarkably strong, conserved synteny since this duplication event, as well as between Myxocyprinus and an unduplicated outgroup, zebrafish (Danio rerio). Gene content and repetitive elements are also approximately evenly distributed across homeologous chromosomes, suggesting that both subgenomes retain some function, with no obvious bias in gene fractionation or subgenome dominance. The Cat-4R duplication provides another independent example of genome evolution following WGD in animals, in this case at the extreme end of conserved genome architecture over at least 25.2 Myr since the duplication. The M. asiaticus genome is a useful resource for researchers interested in understanding genome evolution following WGD in animals.

Retroviral integrations contribute to elevated host cancer rates during germline invasion.

Repeated retroviral infections of vertebrate germlines have made endogenous retroviruses ubiquitous features of mammalian genomes. However, millions of years of evolution obscure many of the immediate repercussions of retroviral endogenisation on host health. Here we examine retroviral endogenisation during its earliest stages in the koala (Phascolarctos cinereus), a species undergoing germline invasion by koala retrovirus (KoRV) and affected by high cancer prevalence. We characterise KoRV integration sites (IS) in tumour and healthy tissues from 10 koalas, detecting 1002 unique IS, with hotspots of integration occurring in the vicinity of known cancer genes. We find that tumours accumulate novel IS, with proximate genes over-represented for cancer associations. We detect dysregulation of genes containing IS and identify a highly-expressed transduced oncogene. Our data provide insights into the tremendous mutational load suffered by the host during active retroviral germline invasion, a process repeatedly experienced and overcome during the evolution of vertebrate lineages.

Structure, gene order, and nucleotide composition of mitochondrial genomes in parasitic lice from Amblycera.

Parasitic lice have unique mitochondrial (mt) genomes characterized by rearranged gene orders, variable genome structures, and less AT content compared to most other insects. However, relatively little is known about the mt genomes of Amblycera, the suborder sister to all other parasitic lice. Comparing among nine different genera (including representative of all seven families), we show that Amblycera have variable and highly rearranged mt genomes. Some genera have fragmented genomes that vary considerably in length, whereas others have a single mt chromosome. Notably, these genomes are more AT-biased than most other lice. We also recover genus-level phylogenetic relationships among Amblycera that are consistent with those reported from large nuclear datasets, indicating that mt sequences are reliable for reconstructing evolutionary relationships in Amblycera. However, gene order data cannot reliably recover these same relationships. Overall, our results suggest that the mt genomes of lice, already know to be distinctive, are even more variable than previously thought.

Head Shape Modulates Diversification of a Classic Cichlid Pharyngeal Jaw Innovation.

Functional innovations are often invoked to explain the uneven distribution of ecological diversity. Innovations may provide access to new adaptive zones by expanding available ecological opportunities and may serve as catalysts of adaptive radiation. However, diversity is often unevenly distributed within clades that share a key innovation, highlighting the possibility that the impact of the innovation is mediated by other traits. Pharyngognathy is a widely recognized innovation of the pharyngeal jaws that enhances the ability to process hard and tough prey in several major radiations of fishes, including marine wrasses and freshwater cichlids. We explored diversification of lower pharyngeal jaw shape, a key feature of pharyngognathy, and the extent to which it is influenced by head shape in Neotropical cichlids. While pharyngeal jaw shape was unaffected by either head length or head depth, its disparity declined dramatically with increasing head width. Head width also predicted the rate of pharyngeal jaw evolution such that higher rates were associated with narrow heads. Wide heads are associated with exploiting prey that require intense processing by pharyngeal jaws that have expanded surfaces for the attachment of enlarged muscles. However, we show that a wide head constrains access to adaptive peaks associated with several trophic roles. A constraint on the independent evolution of pharyngeal jaw and head shape may explain the uneven distribution of ecological diversity within a clade that shares a major functional innovation.

Phylogenetic classification of extant genera of fishes of the order Cypriniformes (Teleostei: Ostariophysi).

The order Cypriniformes is the most diverse order of freshwater fishes. Recent phylogenetic studies have approached a consensus on the phylogenetic relationships of Cypriniformes and proposed a new phylogenetic classification of family-level groupings in Cypriniformes. The lack of a reference for the placement of genera amongst families has hampered the adoption of this phylogenetic classification more widely. We herein provide an updated compilation of the membership of genera to suprageneric taxa based on the latest phylogenetic classifications. We propose a new taxon: subfamily Esominae within Danionidae, for the genus Esomus.

Island- and lake-like parallel adaptive radiations replicated in rivers.

Parallel adaptive radiations have arisen following the colonization of islands by lizards and lakes by fishes. In these classic examples, parallel adaptive radiation is a response to the ecological opportunities afforded by the colonization of novel ecosystems and similar adaptive landscapes that favour the evolution of similar suites of ecomorphs, despite independent evolutionary histories. Here, we demonstrate that parallel adaptive radiations of cichlid fishes arose in South American rivers. Speciation-assembled communities of pike cichlids (Crenicichla) have independently diversified into similar suites of novel ecomorphs in the Uruguay and Paraná Rivers, including crevice feeders, periphyton grazers and molluscivores. There were bursts in phenotypic evolution associated with the colonization of each river and the subsequent expansion of morphospace following the evolution of the ecomorphs. These riverine clades demonstrate that characteristics emblematic of textbook parallel adaptive radiations of island- and lake-dwelling assemblages are feasible evolutionary outcomes even in labile ecosystems such as rivers.

Ecological opportunity alters the timing and shape of adaptive radiation.

The uneven distribution of diversity is a conspicuous phenomenon across the tree of life. Ecological opportunity is a prominent catalyst of adaptive radiation and therefore may alter patterns of diversification. We evaluated the distribution of shifts in diversification rates across the cichlid phylogeny and the distribution of major clades across phylogenetic space. We also tested if ecological opportunity influenced these patterns. Colonization-associated ecological opportunity altered the tempo and mode of diversification during the adaptive radiation of cichlid fishes. Clades that arose following colonization events diversified faster than other clades. Speciation rate shifts were nonrandomly distributed across the phylogeny such that they were disproportionally concentrated around nodes that corresponded with colonization events (i.e., of continents, river basins, or lakes). Young clades tend to expand faster than older clades; however, colonization-associated ecological opportunity accentuated this pattern. There was an interaction between clade age and ecological opportunity that explained the trajectory of clades through phylogenetic space over time. Our results indicate that ecological opportunities afforded by continental and ecosystem-scale colonization events explain the dramatic speciation rate heterogeneity and phylogenetic imbalance that arose during the evolutionary history of cichlid fishes.

Draft sequencing and assembly of the genome of the world's largest fish, the whale shark: Rhincodon typus Smith 1828.

BACKGROUND: The whale shark (Rhincodon typus) has by far the largest body size of any elasmobranch (shark or ray) species. Therefore, it is also the largest extant species of the paraphyletic assemblage commonly referred to as fishes. As both a phenotypic extreme and a member of the group Chondrichthyes - the sister group to the remaining gnathostomes, which includes all tetrapods and therefore also humans - its genome is of substantial comparative interest. Whale sharks are also listed as an endangered species on the International Union for Conservation of Nature's Red List of threatened species and are of growing popularity as both a target of ecotourism and as a charismatic conservation ambassador for the pelagic ecosystem. A genome map for this species would aid in defining effective conservation units and understanding global population structure. RESULTS: We characterised the nuclear genome of the whale shark using next generation sequencing (454, Illumina) and de novo assembly and annotation methods, based on material collected from the Georgia Aquarium. The data set consisted of 878,654,233 reads, which yielded a draft assembly of 1,213,200 contigs and 997,976 scaffolds. The estimated genome size was 3.44Gb. As expected, the proteome of the whale shark was most closely related to the only other complete genome of a cartilaginous fish, the holocephalan elephant shark. The whale shark contained a novel Toll-like-receptor (TLR) protein with sequence similarity to both the TLR4 and TLR13 proteins of mammals and TLR21 of teleosts. The data are publicly available on GenBank, FigShare, and from the NCBI Short Read Archive under accession number SRP044374. CONCLUSIONS: This represents the first shotgun elasmobranch genome and will aid studies of molecular systematics, biogeography, genetic differentiation, and conservation genetics in this and other shark species, as well as providing comparative data for studies of evolutionary biology and immunology across the jawed vertebrate lineages.

Resolving Cypriniformes relationships using an anchored enrichment approach.

BACKGROUND: Cypriniformes (minnows, carps, loaches, and suckers) is the largest group of freshwater fishes in the world (~4300 described species). Despite much attention, previous attempts to elucidate relationships using molecular and morphological characters have been incongruent. In this study we present the first phylogenomic analysis using anchored hybrid enrichment for 172 taxa to represent the order (plus three out-group taxa), which is the largest dataset for the order to date (219 loci, 315,288 bp, average locus length of 1011 bp). RESULTS: Concatenation analysis establishes a robust tree with 97 % of nodes at 100 % bootstrap support. Species tree analysis was highly congruent with the concatenation analysis with only two major differences: monophyly of Cobitoidei and placement of Danionidae. CONCLUSIONS: Most major clades obtained in prior molecular studies were validated as monophyletic, and we provide robust resolution for the relationships among these clades for the first time. These relationships can be used as a framework for addressing a variety of evolutionary questions (e.g. phylogeography, polyploidization, diversification, trait evolution, comparative genomics) for which Cypriniformes is ideally suited.

Two new species of spotted Hypancistrus from the Rio Negro drainage (Loricariidae, Hypostominae).

Two new species, Hypancistrus phantasma and Hypancistrus margaritatus, are described based on material from the Rio Negro drainage. Both species are distinguished from congeners by unique color patterns. Hypancistrus phantasma is described from the Rio Uaupes and differs from congeners by having a tan body with small dark spots (vs. dark with light spots or with saddles or stripes). Hypancistrus margaritatus is described from the Takutu River and differs from congeners by having densely-packed light spots on a dark brown background, with spots about the size of the nasal aperture (vs. sparse light spots either smaller or larger than the nasal aperture, or brown to black spots, saddles, or stripes).

A new species of Panaqolus (Siluriformes: Loricariidae) from the rio Branco

A new species of Panaqolus is described from material from the Takutu River and the mainstem rio Branco. The new species is diagnosed from congeners by its color pattern consisting of dark and light bars on the body, bands on the fins, and with dots and vermiculations absent (vs. no bars in P. albomaculatus , P. nix , P. nocturnus , and P. koko , vs. fins unbanded in P. albomaculatus , P. dentex , P. koko , and P. nix , and vs. dots and vermiculations present in P. albivermis and P. maccus ). The new species is diagnosed from barred species of Panaqolus by its specific bar number and orientation and color pattern on its head, with bars oriented in a anteroventral-posterodorsal direction (vs. anterodorsal-posteroventral bars in P. gnomus ), having consistently 5 bars (n = 4) on the trunk that do not increase with size (vs. number increasing with size in P. purusiensis and vs. 6-12 in P. changae ), and the color pattern on the head of straight lines extending from posterior to the eye to the snout margin, splitting in the middle portion of the line in larger specimens (vs. small, dense reticulate lines in P. changae ). Biogeographically, we infer that the new species ancestrally originated in the Amazon river, dispersing to the Takutu River after the Amazon captured part of the Proto-Berbice.

Uma espécie nova de Panaqolus é descrita do rio Branco e seu afluente, rio Tacutu. A nova espécie é diagnosticada de suas congêneres pelo padrão de colorido composto por barras escuras e claras alternadas no corpo e nadadeiras, não formando máculas ou vermiculações nas nadadeiras (vs. sem barras no corpo em P. albomaculatus , P. nix , P. nocturnus , e P. koko , e vs. sem barras nas nadadeiras em P. albomaculatus , P. dentex , P. koko , e P. nix , e vs. máculas e vermiculações presentes em P. albivermis e P. maccus ). A nova espécie é diagnosticada das espécies de Panaqolus com barras pelo número e orientação das barras e pelo padrão de colorido cefálico, com as barras orientadas posterodorsalmente (vs. posteroventralmente em P. gnomus ), pela presença de cinco barras (n = 4) no tronco que não aumentam com o tamanho (vs. número aumentando com o tamanho em P. purusiensis e vs. 6-12 barras em P. changae ), e o padrão de colorido cefálico composto por linhas retas da margem posterior do olho à margem do focinho, dividida medianamente em indivíduos maiores (vs. linhas pequenas e vermiculadas em P. changae ). Nos inferimos que a nova espécie originou-se ancestralmente no rio Amazonas, dispersando para o rio Tacutu após o Amazonas capturar parte do Proto-Berbice.

Three new species of saddled loricariid catfishes, and a review of Hemiancistrus, Peckoltia, and allied genera (Siluriformes).

Three new species of saddled hypostomine loricariids are described. According to a recent phylogenetic analysis, these species are members of the genus Peckoltia. The species differ from all described Peckoltia except Peckoltiafurcata and Peckoltiasabaji by having the dentaries meet at an angle greater than 90°. The species also have similarities to Hemiancistrus, and can be separated from all described species by having dorsal saddles. We discuss the taxonomy of Peckoltia, Hemiancistrus, and allied genera and recognize Ancistomus as valid for Peckoltiafeldbergae, Hemiancistrusmicrommatos, Ancistrussnethlageae, Hemiancistrusspilomma, and Hemiancistrusspinosissimus. We recommend descriptions of genera for several clades of Hemiancistrus and restriction of Hemiancistrus to the type species of the genus, Hemiancistrusmedians. Chaetostomusmacrops is transferred to Pseudancistrus and recognized as a junior synonym of Pseudancistrusmegacephalus. The Hemiancistrusannectens group of species (Hemiancistrusannectens, Hemiancistrusargus, Hypostomusaspidolepis, Hemiancistrusfugleri, Hemiancistrusholostictus, Hemiancistrusmaracaiboensis, Hemiancistruspanamensis, Hemiancistruswilsoni) are recognized in Hypostomus. Multivariate analysis reveals that the newly described species differ from one another in shape space, but overlap broadly with other Peckoltia (Peckoltialujani), narrowly with other Peckoltia (Peckoltiagreedoi), or broadly with Etsaputu (Peckoltiaephippiata).