A reconstruction of parasite burden reveals one century of climate-associated parasite decline.

Long-term data allow ecologists to assess trajectories of population abundance. Without this context, it is impossible to know whether a taxon is thriving or declining to extinction. For parasites of wildlife, there are few long-term data-a gap that creates an impediment to managing parasite biodiversity and infectious threats in a changing world. We produced a century-scale time series of metazoan parasite abundance and used it to test whether parasitism is changing in Puget Sound, United States, and, if so, why. We performed parasitological dissection of fluid-preserved specimens held in natural history collections for eight fish species collected between 1880 and 2019. We found that parasite taxa using three or more obligately required host species-a group that comprised 52% of the parasite taxa we detected-declined in abundance at a rate of 10.9% per decade, whereas no change in abundance was detected for parasites using one or two obligately required host species. We tested several potential mechanisms for the decline in 3+-host parasites and found that parasite abundance was negatively correlated with sea surface temperature, diminishing at a rate of 38% for every 1 °C increase. Although the temperature effect was strong, it did not explain all variability in parasite burden, suggesting that other factors may also have contributed to the long-term declines we observed. These data document one century of climate-associated parasite decline in Puget Sound-a massive loss of biodiversity, undetected until now.

Alternating regimes of shallow and deep-sea diversification explain a species-richness paradox in marine fishes.

The deep sea contains a surprising diversity of life, including iconic fish groups such as anglerfishes and lanternfishes. Still, >65% of marine teleost fish species are restricted to the photic zone <200 m, which comprises less than 10% of the ocean's total volume. From a macroevolutionary perspective, this paradox may be explained by three hypotheses: 1) shallow water lineages have had more time to diversify than deep-sea lineages, 2) shallow water lineages have faster rates of speciation than deep-sea lineages, or 3) shallow-to-deep sea transition rates limit deep-sea richness. Here we use phylogenetic comparative methods to test among these three non-mutually exclusive hypotheses. While we found support for all hypotheses, the disparity in species richness is better described as the uneven outcome of alternating phases that favored shallow or deep diversification over the past 200 million y. Shallow marine teleosts became incredibly diverse 100 million y ago during a period of warm temperatures and high sea level, suggesting the importance of reefs and epicontinental settings. Conversely, deep-sea colonization and speciation was favored during brief episodes when cooling temperatures increased the efficiency of the ocean's carbon pump. Finally, time-variable ecological filters limited shallow-to-deep colonization for much of teleost history, which helped maintain higher shallow richness. A pelagic lifestyle and large jaws were associated with early deep-sea colonists, while a demersal lifestyle and a tapered body plan were typical of later colonists. Therefore, we also suggest that some hallmark characteristics of deep-sea fishes evolved prior to colonizing the deep sea.

Increasing the impact of vertebrate scientific collections through 3D imaging: The openVertebrate (oVert) Thematic Collections Network.

The impact of preserved museum specimens is transforming and increasing by three-dimensional (3D) imaging that creates high-fidelity online digital specimens. Through examples from the openVertebrate (oVert) Thematic Collections Network, we describe how we created a digitization community dedicated to the shared vision of making 3D data of specimens available and the impact of these data on a broad audience of scientists, students, teachers, artists, and more. High-fidelity digital 3D models allow people from multiple communities to simultaneously access and use scientific specimens. Based on our multiyear, multi-institution project, we identify significant technological and social hurdles that remain for fully realizing the potential impact of digital 3D specimens.

Exon-capture data and locus screening provide new insights into the phylogeny of flatfishes (Pleuronectoidei).

There is an extensive collection of literature on the taxonomy and phylogenetics of flatfishes (Pleuronectiformes) that extends over two centuries, but consensus on many of their evolutionary relationships remains elusive. Phylogenetic uncertainty stems from highly divergent results derived from morphological and genetic characters, and between various molecular datasets. Deciphering relationships is complicated by rapid diversification early in the Pleuronectiformes tree and an abundance of studies that incompletely and inconsistently sample taxa and genetic markers. We present phylogenies based on a genome-wide dataset (4,434 nuclear markers via exon-capture) and wide taxon sampling (86 species spanning 12 of 16 families) of the largest flatfish suborder (Pleuronectoidei). Nine different subsets of the data and two tree construction approaches (eighteen phylogenies in total) are remarkably consistent with other recent molecular phylogenies, and show strong support for the monophyly of all families included except Pleuronectidae. Analyses resolved a novel phylogenetic hypothesis for the family Rhombosoleidae as being within the Pleuronectoidea rather than the Soleoidea, and failed to support the subfamily Hippoglossinae as a monophyletic group. Our results were corroborated with evidence from previous phylogenetic studies to outline regions of persistent phylogenetic uncertainty and identify groups in need of further phylogenetic inference.

Confronting Sources of Systematic Error to Resolve Historically Contentious Relationships: A Case Study Using Gadiform Fishes (Teleostei, Paracanthopterygii, Gadiformes).

Reliable estimation of phylogeny is central to avoid inaccuracy in downstream macroevolutionary inferences. However, limitations exist in the implementation of concatenated and summary coalescent approaches, and Bayesian and full coalescent inference methods may not yet be feasible for computation of phylogeny using complicated models and large data sets. Here, we explored methodological (e.g., optimality criteria, character sampling, model selection) and biological (e.g., heterotachy, branch length heterogeneity) sources of systematic error that can result in biased or incorrect parameter estimates when reconstructing phylogeny by using the gadiform fishes as a model clade. Gadiformes include some of the most economically important fishes in the world (e.g., Cods, Hakes, and Rattails). Despite many attempts, a robust higher-level phylogenetic framework was lacking due to limited character and taxonomic sampling, particularly from several species-poor families that have been recalcitrant to phylogenetic placement. We compiled the first phylogenomic data set, including 14,208 loci ($>$2.8 M bp) from 58 species representing all recognized gadiform families, to infer a time-calibrated phylogeny for the group. Data were generated with a gene-capture approach targeting coding DNA sequences from single-copy protein-coding genes. Species-tree and concatenated maximum-likelihood (ML) analyses resolved all family-level relationships within Gadiformes. While there were a few differences between topologies produced by the DNA and the amino acid data sets, most of the historically unresolved relationships among gadiform lineages were consistently well resolved with high support in our analyses regardless of the methodological and biological approaches used. However, at deeper levels, we observed inconsistency in branch support estimates between bootstrap and gene and site coefficient factors (gCF, sCF). Despite numerous short internodes, all relationships received unequivocal bootstrap support while gCF and sCF had very little support, reflecting hidden conflict across loci. Most of the gene-tree and species-tree discordance in our study is a result of short divergence times, and consequent lack of informative characters at deep levels, rather than incomplete lineage sorting. We use this phylogeny to establish a new higher-level classification of Gadiformes as a way of clarifying the evolutionary diversification of the order. We recognize 17 families in five suborders: Bregmacerotoidei, Gadoidei, Ranicipitoidei, Merluccioidei, and Macrouroidei (including two subclades). A time-calibrated analysis using 15 fossil taxa suggests that Gadiformes evolved $\sim $79.5 Ma in the late Cretaceous, but that most extant lineages diverged after the Cretaceous-Paleogene (K-Pg) mass extinction (66 Ma). Our results reiterate the importance of examining phylogenomic analyses for evidence of systematic error that can emerge as a result of unsuitable modeling of biological factors and/or methodological issues, even when data sets are large and yield high support for phylogenetic relationships. [Branch length heterogeneity; Codfishes; commercial fish species; Cretaceous-Paleogene (K-Pg); heterotachy; systematic error; target enrichment.].

Phylogenomic analysis on the exceptionally diverse fish clade Gobioidei (Actinopterygii: Gobiiformes) and data-filtering based on molecular clocklikeness.

The use of genome-scale data to infer phylogenetic relationships has gained in popularity in recent years due to the progress made in target-gene capture and sequencing techniques. Data filtering, the approach of excluding data inconsistent with the model from analyses, presumably could alleviate problems caused by systematic errors in phylogenetic inference. Different data filtering criteria, such as those based on evolutionary rate and molecular clocklikeness as well as others have been proposed for selecting useful phylogenetic markers, yet few studies have tested these criteria using phylogenomic data. We developed a novel set of single-copy nuclear coding markers to capture thousands of target genes in gobioid fishes, a species-rich lineages of vertebrates, and tested the effects of data-filtering methods based on substitution rate and molecular clocklikeness while attempting to control for the compounding effects of missing data and variation in locus length. We found that molecular clocklikeness was a better predictor than overall substitution rate for phylogenetic usefulness of molecular markers in our study. In addition, when the 100 best ranked loci for our predictors were concatenated and analyzed using maximum likelihood, or combined in a coalescent-based species-tree analysis, the resulting trees showed a well-resolved topology of Gobioidei that mostly agrees with previous studies. However, trees generated from the 100 least clocklike frequently recovered conflicting, and in some cases clearly erroneous topologies with strong support, thus indicating strong systematic biases in those datasets. Collectively these results suggest that data filtering has the potential improve the performance of phylogenetic inference when using both a concatenation approach as well as methods that rely on input from individual gene trees (i.e. coalescent species-tree approaches), which may be preferred in scenarios where incomplete lineage sorting is likely to be an issue.

Repeated invasions into the twilight zone: evolutionary origins of a novel assemblage of fishes from deep Caribbean reefs.

Mesophotic and deeper reefs of the tropics are poorly known and underexplored ecosystems worldwide. Collectively referred to as the 'twilight zone', depths below ~30-50 m are home to many species of reef fishes that are absent from shallower depths, including many undescribed and endemic species. We currently lack even a basic understanding of the diversity and evolutionary origins of fishes on tropical mesophotic reefs. Recent submersible collections in the Caribbean have provided new specimens that are enabling phylogenetic reconstructions that incorporate deep-reef representatives of tropical fish genera. Here, we investigate evolutionary depth transitions in the family Gobiidae (gobies), the most diverse group of tropical marine fishes. Using divergence-time estimation coupled with stochastic character mapping to infer the timing of shallow-to-deep habitat transitions in gobies, we demonstrate at least four transitions from shallow to mesophotic depths. Habitat transitions occurred in two broad time periods (Miocene, Pliocene-Pleistocene), and may have been linked to the availability of underutilized niches, as well as the evolution of morphological/behavioural adaptations for life on deep reefs. Further, our analysis shows that at least three evolutionary lineages that invaded deep habitats subsequently underwent speciation, reflecting another unique mode of radiation within the Gobiidae. Lastly, we synthesize depth distributions for 95 species of Caribbean gobies, which reveal major bathymetric faunal breaks at the boundary between euphotic and mesophotic reefs. Ultimately, our study is the first rigorous investigation into the origin of Caribbean deep-reef fishes and provides a framework for future studies that utilize rare, deep-reef specimens.

Support for a 'Center of Origin' in the Coral Triangle: cryptic diversity, recent speciation, and local endemism in a diverse lineage of reef fishes (Gobiidae: Eviota).

The Coral Triangle is widely regarded as the richest marine biodiversity hot-spot in the world. One factor that has been proposed to explain elevated species-richness within the Coral Triangle is a high rate of in situ speciation within the region itself. Dwarfgobies (Gobiidae: Eviota) are a diverse genus of diminutive cryptobenthic reef fishes with limited dispersal ability, and life histories and ecologies that increase potential for speciation. We use molecular phylogenetic and biogeographic data from two clades of Eviota species to examine patterns, processes and timing associated with species origination within the Coral Triangle. Sequence data from mitochondrial and nuclear DNA were used to generate molecular phylogenies and median-joining haplotype networks for the genus Eviota, with emphasis on the E. nigriventris and E. bifasciata complexes - two species groups with distributions centered in the Coral Triangle. The E. nigriventris and E. bifasciata complexes both contain multiple genetically distinct, geographically restricted color morphs indicative of recently-diverged species originating within the Coral Triangle. Relaxed molecular-clock dating estimates indicate that most speciation events occurred within the Pleistocene, and the geographic pattern of genetic breaks between species corresponds well with similar breaks in other marine fishes and sessile invertebrates. Regional isolation due to sea-level fluctuations may explain some speciation events in these species groups, yet other species formed with no evidence of physical isolation. The timing of diversification events and present day distributions of Eviota species within the Coral Triangle suggest that both allopatric speciation (driven by ephemeral and/or 'soft' physical barriers to gene flow) and sympatric speciation (driven by niche partitioning and assortative mating) may be driving diversification at local scales within the Coral Triangle. The presence of multiple young, highly-endemic cryptic species of Eviota within the Coral Triangle suggests that (i) the Coral Triangle is indeed a "cradle" of reef fish biodiversity and that (ii) our current approximations of reef fish diversity in the region may be significantly underestimated.

Eviota brahmi n. sp. from Papua New Guinea, with a redescription of Eviota nigriventris (Teleostei: Gobiidae).

Greenfield & Randall (2011) described the gobiid fishes Eviota dorsogilva from Fiji and E. dorsopurpurea from Papua New Guinea as new species in what they termed the Eviota nigriventris complex. They also extended the range of E. nigriventris, type locality Banda Sea, to Milne Bay, Papua New Guinea. In the present paper, we describe their misidentified E. nigriventris from Papua New Guinea as a new species, E. brahmi, and redescribe E. nigriventris based on new material from near the type locality. The four species of this complex differ mainly in coloration, but are also shown to be distinct using mitochondrial and nuclear DNA.

3D ocean assessments reveal that fisheries reach deep but marine protection remains shallow.

The wave of new global conservation targets, the conclusion of the High Seas Treaty negotiations, and the expansion of extractive use into the deep sea call for a paradigm shift in ocean conservation. The current reductionist 2D representation of the ocean to set targets and measure impacts will fail at achieving effective biodiversity conservation. Here, we develop a framework that overlays depth realms onto marine ecoregions to conduct the first three-dimensional spatial analysis of global marine conservation achievements and fisheries footprint. Our novel approach reveals conservation gaps of mesophotic, rariphotic, and abyssal depths and an underrepresentation of high protection levels across all depths. In contrast, the 3D footprint of fisheries covers all depths, with benthic fishing occurring down to the lower bathyal and mesopelagic fishing peaking in areas overlying abyssal depths. Additionally, conservation efforts are biased towards areas where the lowest fishing pressures occur, compromising the effectiveness of the marine conservation network. These spatial mismatches emphasize the need to shift towards 3D thinking to achieve ocean sustainability.

The Grumpy dwarfgoby, a new species of Sueviota (Teleostei, Gobiidae) from the Red Sea.

A new gobiid species is described from ten specimens, 9.2 - 16.7 mm SL, collected from the Saudi Arabian Red Sea. The new species is most similar to Sueviotapyrios from the Gulf of Aqaba in the northern Red Sea. It differs from S.pyrios by having no large red spots on the dorsal and caudal fin elements, no elongate spines in the first dorsal fin, a shorter pelvic fin that does not reach the anus, branched pectoral fin rays, and a projecting lower jaw. The new species is further distinguished from all its congeners by a complete lack of cephalic sensory canals and pores. Specimens were found in small caves and overhangs at depths between 10 and 53 meters.

Vertical structure of Caribbean deep-reef fishes from the altiphotic to deep-sea boundary.

While recent technical breakthroughs have enabled advances in the description of reefs down to 150 m, the structure and depth zonation of deep-reef communities below 150 m remains largely unknown. Here, we present results from over 10 years of deep-reef fish surveys using human-occupied submersibles at four locations across the Caribbean Sea, constituting one of the only continuous reef-fish surveys from 10 to 480 m (1 site) and 40 to 300 m (3 sites). We identify four vertically stratified deep-reef fish communities between 40 and 300 m bordered by an altiphotic (0-10 m) and a deep-sea (300-480 m) community. We found a strong faunal break around 150 m that separates mesophotic and rariphotic zones and secondary breaks at ~ 70 to 90 m and ~ 180 to 200 m subdividing these zones into upper and lower communities. From 300 to 480 m in Roatán, we found a single fish community dominated by deep-sea families, indicating that the lower boundary of the reef-fish realm occurs at 300 m. No differences were found between communities ranging from 20 to 60 m, suggesting that fishes from the lower altiphotic and upper mesophotic form an ecological continuum. While some variability was observed across sites, the overall depth zonation and key species characterizing depth zones were consistent. Most deep-reef species observed were depth specialists restricted to a single depth zone, but many shallow-reef species extended down to mesophotic depths. Depth segregation among species of a genus was found across ten reef-fish genera and likely constitutes one of the mechanisms driving community distinctiveness and thereby fish diversity across depths.

Evolution of microhabitat association and morphology in a diverse group of cryptobenthic coral reef fishes (Teleostei: Gobiidae: Eviota).

Gobies (Teleostei: Gobiidae) are an extremely diverse and widely distributed group and are the second most species rich family of vertebrates. Ecological drivers are key to the evolutionary success of the Gobiidae. However, ecological and phylogenetic data are lacking for many diverse genera of gobies. Our study investigated the evolution of microhabitat association across the phylogeny of 18 species of dwarfgobies (genus Eviota), an abundant and diverse group of coral reef fishes. In addition, we also explore the evolution of pectoral fin-ray branching and sensory head pores to determine the relationship between morphological evolution and microhabitat shifts. Our results demonstrate that Eviota species switched multiple times from a facultative hard-coral association to inhabiting rubble or mixed sand/rubble habitat. We found no obvious relationship between microhabitat shifts and changes in pectoral fin-ray branching or reduction in sensory pores, with the latter character being highly homoplasious throughout the genus. The relative flexibility in coral-association in Eviota combined with the ability to move into non-coral habitats suggests a genetic capacity for ecological release in contrast to the strict obligate coral-dwelling relationship commonly observed in closely related coral gobies, thus promoting co-existence through fine scale niche partitioning. The variation in microhabitat association may facilitate opportunistic ecological speciation, and species persistence in the face of environmental change. This increased speciation opportunity, in concert with a high resilience to extinction, may explain the exceptionally high diversity seen in Eviota compared to related genera in the family.

Two new species of Varicus from Caribbean deep reefs, with comments on the related genus Pinnichthys (Teleostei, Gobiidae, Gobiosomatini, Nes subgroup).

Tropical deep reefs (~40-300 m) are diverse ecosystems that serve as habitats for diverse communities of reef-associated fishes. Deep-reef fish communities are taxonomically and ecologically distinct from those on shallow reefs, but like those on shallow reefs, they are home to a species-rich assemblage of small, cryptobenthic reef fishes, including many species from the family Gobiidae (gobies). Here we describe two new species of deep-reef gobies, Varicusprometheussp. nov. and V.roatanensissp. nov., that were collected using the submersible Idabel from rariphotic reefs off the island of Roatan (Honduras) in the Caribbean. The new species are the 11th and 12th species of the genus Varicus, and their placement in the genus is supported by morphological data and molecular phylogenetic analyses. Additionally, we also collected new specimens of the closely-related genus and species Pinnichthysaimoriensis during submersible collections off the islands of Bonaire and St. Eustatius (Netherland Antilles) and included them in this study to expand the current description of that species and document its range extension from Brazil into the Caribbean. Collectively, the two new species of Varicus and new records of P.aimoriensis add to our growing knowledge of cryptobenthic fish diversity on deep reefs of the Caribbean.

A review of the Eviotazebrina complex, with descriptions of four new species (Teleostei, Gobiidae).

The Eviotazebrina complex includes eight species of closely-related dwarfgobies, four of which are herein described as new. The complex is named for Eviotazebrina Lachner & Karnella, 1978, an Indian Ocean species with the holotype from the Seychelles Islands and also known from the Maldives, which was once thought to range into the Gulf of Aqaba and the Red Sea eastward to the Great Barrier Reef of Australia. Our analysis supports the recognition of four genetically distinct, geographically non-overlapping, species within what was previously called E.zebrina, with E.zebrina being restricted to the Indian Ocean, E.marerubrum sp. nov. described from the Red Sea, E.longirostris sp. nov. described from western New Guinea, and E.pseudozebrina sp. nov. described from Fiji. The caudal fin of all four of these species is crossed by oblique black bars in preservative, but these black bars are absent from the four other species included in the complex. Two of the other species within the complex, E.tetha and E.gunawanae are morphologically similar to each other in having the AITO cephalic-sensory pore positioned far forward and opening anteriorly. Eviotatetha is known from lagoonal environments in Cenderawasih Bay and Raja Ampat, West Papua, and E.gunawanae is known only from deeper reefs (35-60 m) from Fakfak Regency, West Papua. The final two species are E.cometa which is known from Fiji and Tonga and possesses red bars crossing the caudal fin (but lost in preservative) and a 9/8 dorsal/anal-fin formula, and E.oculineata sp. nov., which is described as new from New Guinea and the Solomon Islands, and possesses an 8/7 dorsal/anal-fin formula and lacks red caudal bars. Eviotaoculineata has been confused with E.cometa in the past.

A new species of Hetereleotris (Teleostei: Gobiidae) from the Socotra Archipelago (north-western Indian Ocean), a rare case of a hole-associated adaptation in gobiid fishes.

A new cryptobenthic gobiid species Hetereleotris nasoramosa sp. nov. is described based on the holotype and five paratypes collected from the north-eastern part of Socotra Island, Arabian Sea, from moderately large pieces of coral rocks with holes at depths of 811 m. Molecular phylogenetic analysis placed the new species within the genus Hetereleotris. Hetereleotris nasoramosa sp. nov., differs from all species of Hetereleotris in having developed tentacles extending from each anterior and posterior nostril and five transverse suborbital papillae rows (instead four or six in other species). The new species superficially resembles the recently described Red Sea endemic species Cerogobius petrophilus by having forward-set, elevated eyes, a short snout, a moderately large mouth, a relatively deep and short caudal peduncle, and developed tentacles on the head, but differs from it by the same characters of developed tentacles extending from each anterior and posterior nostril and five transverse suborbital papillae rows as from other Hetereleotris species. Both species also share a specific habitat preference for tight holes in rock covered by micro-algae. A full description of the species is provided as well as a revised key to the species of Hetereleotris.

Corrigenda: A new species of Chromis damselfish from the tropical western Atlantic (Teleostei, Pomacentridae). ZooKeys 1008: 107-138. https://zookeys.pensoft.net/article/58805/.

[This corrects the article DOI: 10.3897/zookeys.1008.58805.].

Fluid-preserved fishes are one solution for assessing historical change in fish trophic level.

There are few resources available for assessing historical change in fish trophic dynamics, but specimens held in natural history collections could serve as this resource. In contemporary trophic ecology studies, trophic and source information can be obtained from compound-specific stable isotope analysis of amino acids of nitrogen (CSIA-AA-N).We subjected whole Sebastes ruberrimus and Clupea pallasii to formalin fixation and 70% ethanol preservation. We extracted tissue samples from each fish pre-fixation, after each chemical change, and then in doubling time for 32-64 days once placed in the final preservative. All samples were subjected to CSIA-AA-N, and their glutamic acid and phenylalanine profiles and associated trophic position were examined for differences over time by species.Glutamic acid and phenylalanine values were inconsistent in direction and magnitude, particularly during formalin fixation, but stabilized similarly (in 70% ethanol) among conspecifics. In some cases, the amino acid values of our final samples were significantly different than our initial pre-preservation samples. Nonetheless, significant differences in glutamic acid, phenylalanine, and estimated trophic position were not detected among samples that were in 70% ethanol for >24 hr.Our results suggest that the relative trophic position of fluid-preserved specimens can be estimated using CSIA-AA-N, and CSIA-AA-N estimates for fluid-preserved specimens should only be reported as relative differences. Timelines of trophic position change can be developed by comparing specimens collected at different points in time, revealing trophic information of the past and cryptic ecosystem responses.

Co-evolution of cleaning and feeding morphology in western Atlantic and eastern Pacific gobies.

Cleaning symbioses are mutualistic relationships where cleaners remove and consume ectoparasites from their clients. Cleaning behavior is rare in fishes and is a highly specialized feeding strategy only observed in around 200 species. Cleaner fishes vary in their degree of specialization, ranging from species that clean as juveniles or facultatively as adults, to nearly obligate or dedicated cleaners. Here, we investigate whether these different levels of trophic specialization correspond with similar changes in feeding morphology. Specifically, we model the evolution of cleaning behavior across the family Gobiidae, which contains the most speciose radiation of dedicated and facultative cleaner fishes. We compared the cranial morphology and dentition of cleaners and non-cleaners across the phylogeny of cleaning gobies and found that facultative cleaners independently evolved four times and have converged on an intermediate morphology relative to that of dedicated cleaners and non-cleaning generalists. This is consistent with their more flexible feeding habits. Cleaner gobies also possess a distinct tooth morphology, which suggests they are adapted for scraping parasites off their clients and show little similarity to other cleaner clades. We propose that evolutionary history and pre-adaptation underlie the morphological and ecological diversification of cleaner fishes.