Sex-related differences in aging rate are associated with sex chromosome system in amphibians.

Sex-related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture-recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex-specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the "unguarded X/Z effect") or repeat-rich Y/W chromosome (the "toxic Y/W effect") could accelerate aging in the heterogametic sex in some vertebrate clades.

Nickel toxicity in wood frog tadpoles: Bioaccumulation and sublethal effects on body condition, food consumption, activity, and chemosensory function.

Nickel (Ni) concentrations in aquatic ecosystems can be amplified by anthropogenic activities including resource extraction. Compared with fish and invertebrates, knowledge of Ni toxicity in amphibians is limited, especially for northern species. We examined the effect of Ni on wood frog (Lithobates sylvaticus) tadpoles, the species with the widest and most northern distribution of any anuran in North America. Wood frog tadpoles were exposed to a Ni concentration gradient (0.02-5.5 mg/L of Ni at 164 mg/L as CaCO3 water hardness) for 8 d and examined for lethality, Ni bioaccumulation, and several sublethal endpoints including body condition, food consumption, activity, and chemosensory function. Nickel induced a sublethal effect on body condition (8-d 10 and 20% effect concentrations [EC10 and EC20] of 1.07 ± 0.38 and 2.44 ± 0.51 mg/L of Ni ± standard error [SE], respectively) but not on food consumption, activity, or chemosensory function. Nickel accumulation in tadpole tissues was positively related to an increase in aqueous Ni concentration but was not lethal. Both the acute and chronic US Environmental Protection Agency water quality guideline concentrations for Ni (0.71 and 0.08 mg/L at 164 mg/L as CaCO3 water hardness, respectively) were protective against lethal and sublethal effects in wood frog tadpoles. In the present study, wood frog tadpoles were protected by current water quality guidelines for Ni and are likely not as useful as other taxa for environmental effects monitoring for this particular metal. Environ Toxicol Chem 2018;37:2458-2466. © 2018 SETAC.

Prevalence and Seasonality of the Amphibian Chytrid Fungus Batrachochytrium dendrobatidis Along Widely Separated Longitudes Across the United States.

The chytrid fungus Batrachochytrium dendrobatidis (Bd) has been implicated in amphibian declines on almost all continents. We report on prevalence and intensity of Bd in the United States amphibian populations across three longitudinally separated north-to-south transects conducted at 15 Department of Defense installations during two sampling periods (late-spring/early summer and mid to late summer). Such a standardized approach minimizes the effects of sampling and analytical bias, as well as human disturbance (by sampling restricted military bases), and therefore permits a cleaner interpretation of environmental variables known to affect chytrid dynamics such as season, temperature, rainfall, latitude, and longitude. Our prevalence of positive samples was 20.4% (137/670), and our mean intensity was 3.21 zoospore equivalents (SE = 1.03; range 0.001-103.59). Of the 28 amphibian species sampled, 15 tested positive. Three sites had no evidence of Bd infection; across the remaining 12 Bd-positive sites, neither infection prevalence nor intensity varied systematically. We found a more complicated pattern of Bd prevalence than anticipated. Early season samples showed no trend associated with increasing temperature and precipitation and decreasing (more southerly) latitudes; while in late season samples, the proportion of infected individuals decreased with increasing temperature and precipitation and decreasing latitudes. A similar pattern held for the east-west gradient, with the highest prevalence associated with more easterly/recently warmer sites in the early season then shifting to more westerly/recently cooler sites in the later season. Bd intensity across bases and sampling periods was comparatively low. Some of the trends in our data have been seen in previous studies, and our results offer further continental-level Bd sampling over which more concentrated local sampling efforts can be overlaid.

Drought reduces chytrid fungus (Batrachochytrium dendrobatidis) infection intensity and mortality but not prevalence in adult crawfish frogs (Lithobates areolatus).

To fully understand the impacts of the chytrid fungus Batrachochytrium dendrobatidis (Bd) on amphibians it is necessary to examine the interactions between populations and their environment. Ecologic variables can exacerbate or ameliorate Bd prevalence and infection intensity, factors that are positively related when Bd is acting on naive amphibian populations as an epidemic disease. In crawfish frogs (Lithobates areolatus), a North American species with a complex life history, we have shown that Bd acts as an endemic disease with impacts that vary seasonally; the highest infection prevalences and intensities and highest frog mortality occurred during late spring in postbreeding individuals. In this study, conducted between 28 February and 23 August 2011 in southwestern Indiana on the same population, we report an uncoupling of the previously observed relationship between Bd prevalence and intensity following an extreme drought. Specifically, there was a postdrought reduction in Bd infection intensity and mortality, but not in infection prevalence. This result suggests that the relationship between prevalence and intensity observed in Bd epidemics can be uncoupled in populations harboring endemic infections. Further, constant prevalence rates suggest either that crawfish frogs are being exposed to Bd sources independent of ambient moisture or that low-level infections below detection thresholds persist from year to year. Drought has several ecologically beneficial effects for amphibians with complex life histories, including eliminating fish and invertebrate populations that feed on larvae. To these ecologic benefits we suggest another, that drought can reduce the incidence of the severe skin disease (chytridiomycosis) due to Bd infection.

Localized hotspots drive continental geography of abnormal amphibians on U.S. wildlife refuges.

Amphibians with missing, misshapen, and extra limbs have garnered public and scientific attention for two decades, yet the extent of the phenomenon remains poorly understood. Despite progress in identifying the causes of abnormalities in some regions, a lack of knowledge about their broader spatial distribution and temporal dynamics has hindered efforts to understand their implications for amphibian population declines and environmental quality. To address this data gap, we conducted a nationwide, 10-year assessment of 62,947 amphibians on U.S. National Wildlife Refuges. Analysis of a core dataset of 48,081 individuals revealed that consistent with expected background frequencies, an average of 2% were abnormal, but abnormalities exhibited marked spatial variation with a maximum prevalence of 40%. Variance partitioning analysis demonstrated that factors associated with space (rather than species or year sampled) captured 97% of the variation in abnormalities, and the amount of partitioned variance decreased with increasing spatial scale (from site to refuge to region). Consistent with this, abnormalities occurred in local to regional hotspots, clustering at scales of tens to hundreds of kilometers. We detected such hotspot clusters of high-abnormality sites in the Mississippi River Valley, California, and Alaska. Abnormality frequency was more variable within than outside of hotspot clusters. This is consistent with dynamic phenomena such as disturbance or natural enemies (pathogens or predators), whereas similarity of abnormality frequencies at scales of tens to hundreds of kilometers suggests involvement of factors that are spatially consistent at a regional scale. Our characterization of the spatial and temporal variation inherent in continent-wide amphibian abnormalities demonstrates the disproportionate contribution of local factors in predicting hotspots, and the episodic nature of their occurrence.

Do frogs get their kicks on Route 66? Continental U.S. transect reveals spatial and temporal patterns of Batrachochytrium dendrobatidis infection.

The chytrid fungus Batrachochytrium dendrobatidis (Bd) has been devastating amphibians globally. Two general scenarios have been proposed for the nature and spread of this pathogen: Bd is an epidemic, spreading as a wave and wiping out individuals, populations, and species in its path; and Bd is endemic, widespread throughout many geographic regions on every continent except Antarctica. To explore these hypotheses, we conducted a transcontinental transect of United States Department of Defense (DoD) installations along U.S. Highway 66 from California to central Illinois, and continuing eastward to the Atlantic Seaboard along U.S. Interstate 64 (in sum from Marine Corps Base Camp Pendleton in California to Naval Air Station Oceana in Virginia). We addressed the following questions: 1) Does Bd occur in amphibian populations on protected DoD environments? 2) Is there a temporal pattern to the presence of Bd? 3) Is there a spatial pattern to the presence of Bd? and 4) In these limited human-traffic areas, is Bd acting as an epidemic (i.e., with evidence of recent introduction and/or die-offs due to chytridiomycosis), or as an endemic (present without clinical signs of disease)? Bd was detected on 13 of the 15 bases sampled. Samples from 30 amphibian species were collected (10% of known United States' species); half (15) tested Bd positive. There was a strong temporal (seasonal) component; in total, 78.5% of all positive samples came in the first (spring/early-summer) sampling period. There was also a strong spatial component--the eleven temperate DoD installations had higher prevalences of Bd infection (20.8%) than the four arid (<60 mm annual precipitation) bases (8.5%). These data support the conclusion that Bd is now widespread, and promote the idea that Bd can today be considered endemic across much of North America, extending from coast-to-coast, with the exception of remote pockets of naïve populations.

Seasonal pattern of Batrachochytrium dendrobatidis infection and mortality in Lithobates areolatus: affirmation of Vredenburg's "10,000 zoospore rule".

To fully comprehend chytridiomycosis, the amphibian disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), it is essential to understand how Bd affects amphibians throughout their remarkable range of life histories. Crawfish Frogs (Lithobates areolatus) are a typical North American pond-breeding species that forms explosive spring breeding aggregations in seasonal and semipermanent wetlands. But unlike most species, when not breeding Crawfish Frogs usually live singly--in nearly total isolation from conspecifics--and obligately in burrows dug by crayfish. Crayfish burrows penetrate the water table, and therefore offer Crawfish Frogs a second, permanent aquatic habitat when not breeding. Over the course of two years we sampled for the presence of Bd in Crawfish Frog adults. Sampling was conducted seasonally, as animals moved from post-winter emergence through breeding migrations, then back into upland burrow habitats. During our study, 53% of Crawfish Frog breeding adults tested positive for Bd in at least one sample; 27% entered breeding wetlands Bd positive; 46% exited wetlands Bd positive. Five emigrating Crawfish Frogs (12%) developed chytridiomycosis and died. In contrast, all 25 adult frogs sampled while occupying upland crayfish burrows during the summer tested Bd negative. One percent of postmetamorphic juveniles sampled were Bd positive. Zoospore equivalents/swab ranged from 0.8 to 24,436; five out of eight frogs with zoospore equivalents near or >10,000 are known to have died. In summary, Bd infection rates in Crawfish Frog populations ratchet up from near zero during the summer to over 25% following overwintering; rates then nearly double again during and just after breeding--when mortality occurs--before the infection wanes during the summer. Bd-negative postmetamorphic juveniles may not be exposed again to this pathogen until they take up residence in crayfish burrows, or until their first breeding, some years later.

Divergence of brain and retinal anatomy and histology in pelagic antarctic notothenioid fishes of the sister taxa Dissostichus and Pleuragramma.

The neutrally buoyant Antarctic fishes of the sister taxa Dissostichus (D. eleginoides and D. mawsoni) and Pleuragramma antarcticum diverged early in the notothenioid radiation and filled different niches in the pelagic realm of the developing Southern Ocean. To assess the influence of phylogenetic and ecological factors in shaping neural morphology in these taxa, we studied the anatomy and histology of the brains and retinae, and determined the proportional weights of brain regions. With the brain of the non-Antarctic sister taxon Eleginops maclovinus as plesiomorphic, statistically significant departures in the brains of the two Antarctic taxa include reduction of the corpus cerebelli and expansion of the mesencephalon and medulla. Compared to Eleginops, both species also have a relatively smaller telencephalon, although this is significant only in Dissostichus. There are a number of apomorphic features in the brain of Pleuragramma including reduced olfactory nerves and bulbs, an extremely small corpus cerebelli and an expanded mesencephalon. Although there is not a significant difference in the relative weights of the medulla in the two taxa, the prominence of the eminentia granularis and bulging cap-like appearance of the crista cerebellaris are distinctive in Pleuragramma. Brain histology of Dissostichus and Pleuragramma reflects typical perciform patterns and the two species of Dissostichus are histologically identical. Lateral compression in Pleuragramma and notable lobation in Dissostichus also contribute to differences between the taxa. Compression in Pleuragramma is attributable to convergence on an anchovy/herring body shape and to the relatively large brain in this small fish. The less prominent pattern of lobation of the telencephalon, inferior lobes and corpus cerebelli in Pleuragramma probably reflects underlying histology, specifically a reduction in cellularity of the neuropil in the nuclei and lobes. The retinal histology of Dissostichus and Pleuragramma encompasses the extremes seen in Antarctic notothenioids. Dissostichus has a thin scotopic retina with few cones and a high degree of summation. The retina of Pleuragramma is thick and cellular with many small single cones and rods and resembles that of Eleginops. Pedomorphy has not influenced brain morphology in these species but Pleuragramma has superficial neuromasts that are pedomorphic. Although Dissostichus and Pleuragramma are sympatric in the water column, their brains and retinae are highly divergent and reflect the influences of both phylogeny and ecological partitioning of the pelagic realm. Compared to Eleginops, the relatively smaller corpus cerebelli but relatively larger medulla probably indicates, respectively, reduced activity levels of notothenioids in subzero temperatures and expansion of the mechanosensory lateral line system as a supplement to vision under conditions of reduced light. Compared to Dissostichus, Pleuragramma has reduced olfactory bulbs and corpus cerebelli and an expanded mesencephalon. The reduction of the corpus to a small round knob is consistent with physiological parameters and video observations suggesting that, although pelagic, it is relatively inactive. Because mesencephalic weights also include the valvula cerebelli, the relatively large value for Pleuragramma may be attributable to its role in integration and sensorimotor coordination of information from the highly cellular duplex retina and to integration of signals from thewell-developed octavolateralis system. The brain of Dissostichus displays considerable persistent morphology in its overall resemblance to that of Eleginops, especially the large olfactory bulbs and the relatively large caudally projecting corpus, and Dissostichus exhibits olfactory tracking ability and migratory behavior in common with Eleginops.

Brain and sense organ anatomy and histology of the Falkland Islands mullet, Eleginops maclovinus (Eleginopidae), the sister group of the Antarctic notothenioid fishes (Perciformes: Notothenioidei).

The perciform notothenioid fish Eleginops maclovinus, representing the monotypic family Eleginopidae, has a non-Antarctic distribution in the Falkland Islands and southern South America. It is the sister group of the five families and 103 species of Antarctic notothenioids that dominate the cold shelf waters of Antarctica. Eleginops is the ideal subject for documenting the ancestral morphology of nervous and sensory systems that have not had historical exposure to the unusual Antarctic thermal and light regimes, and for comparing these systems with those of the phyletically derived Antarctic species. We present a detailed description of the brain and cranial nerves of Eleginops and ask how does the neural and sensory morphology of this non-Antarctic notothenioid differ from that seen in the phyletically derived Antarctic notothenioids? The brain of Eleginops is similar to those of visually oriented temperate and tropical perciforms. The tectum is smaller but it has well-developed olfactory and mechanoreceptive lateral line areas and a large, caudally projecting corpus cerebellum. Eye diameter is about twofold smaller in Eleginops than in many Antarctic species. Eleginops has a duplex (rod and cone) retina with single and occasional twin cones conspicuous centrally. Ocular vascular structures include a large choroid rete mirabile and a small lentiform body; a falciform process and hyaloid arteries are absent. The olfactory rosette is oval with 50-55 lamellae, a large number for notothenioids. The inconspicuous bony canals of the cephalic lateral line system are simple with membranous secondary branches that lack neuromasts. In Antarctic species, the corpus cerebellum is the most variable brain region, ranging in size from large and caudally projecting to small and round. "Stalked" brains showing reduction in the size of the telencephalon, tectum, and corpus cerebellum are present in the deep-living artedidraconid Dolloidraco longedorsalis and in most of the deep-living members of the Bathydraconini. Eye diameter is generally larger in Antarctic species but there is a phylogenetic loss of cellularity in the retina, including cone photoreceptors. Some deep-living Antarctic species have lost most of their cones. Mechanosensation is expanded in some species, most notably the nototheniid Pleuragramma antarcticum, the artedidraconid genera Dolloidraco and Pogonophryne, and the deep living members of the bathydraconid tribe Bathydraconini. Reduction in retinal cellularity, expansion of mechanoreception, and stalking are the most noteworthy departures from the morphology seen in Eleginops. These features reflect a modest depth or deep-sea effect, and they are not uniquely "Antarctic" attributes. Thus, at the level of organ system morphology, perciform brain and sensory systems are suitable for conditions on the Antarctic shelf, with only minor alterations in structure in directions exhibited by other fish groups inhabiting deep water. Notothenioids retain a relative balance among their array of senses that reflects their heritage as inshore perciforms.

Brain and sense organ anatomy and histology of two species of phyletically basal non-Antarctic thornfishes of the Antarctic suborder Notothenioidei (Perciformes: Bovichtidae).

The predominantly non-Antarctic family Bovichtidae is phyletically basal within the perciform suborder Notothenioidei, the dominant component of the Antarctic fish fauna. In this article we focus on the South Atlantic bovichtids Bovichtus diacanthus, the klipfish from tide pools at Tristan da Cunha, and Cottoperca gobio, the frogmouth from the Patagonian shelf and Falkland Islands. We document the anatomy and histology of the brains, olfactory apparatus, retina, and cephalic lateral line system. We also use the microvascular casting agent Microfil to examine ocular vascular structures. We provide detailed drawings of the brains and cranial nerves of both species. Typical of perciforms, the brains of both species have a well-developed tectum and telencephalon and robust thalamic nuclei. The telencephalon of C. gobio is prominently lobed, with the dorsomedial nucleus more conspicuous than in any other notothenioid. The corpus cerebelli is relatively small and upright and, unlike other notothenioids, has prominent transverse sulci on the dorsal and caudal surfaces. Areas for lateral line mechanoreception (eminentia granularis and crista cerebellaris) are also conspicuous but olfactory, gustatory, and somatosensory areas are less prominent. The anterior lateral line nerve complex is larger than the posterior lateral line nerve in B. diacanthus, and in their cephalic lateral line systems both species possess branched membranous tubules (which do not contain neuromasts) with small pores. These are especially complex in B. diacanthus where they become increasingly branched and more highly pored in progressively larger specimens. Superficial neuromasts are sparse. Both species have duplex (cone and rod) retinae that are 1.25-fold thicker and have nearly 5-fold more photoreceptors and than those of most Antarctic notothenioids. Convergence ratios are also high for bovichtids. Bovichtus diacanthus has a yellow intraocular filter in the dorsal aspect of the cornea. Both species are unique among notothenioids in possessing all three vascular structures present in the generalized teleostean eye: the choroid rete mirabile, the lentiform body (also a rete), and the falciform process. When comparing the phyletically derived Antarctic clade exemplified by the families Artedidraconidae, Bathydraconidae, and Channichthyidae to the phyletically basal bovichtids, we observe phyletic regression and reduction in some regions of the brain and in some sensory modalities that are well displayed in bovichtids. In the phyletically derived families the brain is less cellular and nuclei are smaller and less prominent. In some species reduction in the size of the telencephalon, tectum, and corpus cerebelli imparts a "stalked" appearance to the brain with the neural axis visible between the reduced lobes. There is also a phyletic reduction in the number of ocular vascular structures from three in bovichtids to one or none in artedidraconids, bathydraconids, and channichthyids. There are no morphological features of bovichtid brains and sense organs that presage the divergence of the phyletically derived members of the clade in the Antarctic marine environment with its cold and deep continental shelves. We conclude that this environment does not require sensory or neural morphology or capabilities beyond those provided by the basic perciform body plan.

Brain and sensory organ morphology in Antarctic eelpouts (Perciformes: Zoarcidae: Lycodinae).

Eelpouts of the family Zoarcidae comprise a monophyletic group of marine fishes with a worldwide distribution. Centers of high zoarcid diversity occur in the North Atlantic and North Pacific, with important radiations into the Arctic, along southern South America, and into the Southern Ocean around Antarctica. Along with snailfishes (Liparidae), zoarcids form an important component of the non-notothenioid fauna in the subzero shelf waters of Antarctica. We document the anatomy and histology of the brains, cranial nerves, olfactory apparatus, cephalic lateral lines, taste buds, and retinas of three Antarctic zoarcid species, living at depths of 310-939 m, representing three of the nine genera from this region. The primary emphasis is on Ophthalmolycus amberensis, and we provide a detailed drawing of the brain and cranial nerves of this species. Although this brain reflects general perciform neural morphology, it exhibits a reduction of the (optic) tecta and the eminentia granulares and crista cerebellares of the lateral line system. Interspecific differences among the three species are slight. The olfactory rosette consists of three to four lamellae and the nasal sac, contrary to the claim of Fanta et al. ([2001] Antarct Rec, Natl Inst Polar Res, Tokyo 45:27-42), is not in communication with the cephalic lateral line system. Primary olfactory neurons are abundant and converge on branches of the olfactory nerve. Numerous taste buds are located in the lips. All three species lack an ocular choroid rete and have relatively thin retinas with a low cell density and a single bank of rods as the only type of photoreceptor. Neural diversification among Antarctic zoarcids has not involved the evolution of sensory specialists; brain and sensory organ morphologies do not approach the condition seen in primary deep-sea fishes, or even that of some sympatric non-perciform secondary deep-sea fishes, including liparids and muraenolepidids (eel cods). There may be phylogenetic constraints on brain morphology in perciforms such that we do not see extreme specialization in sensory and neural systems for deep habitats. We suggest that the brains and sensory organs of Antarctic zoarcids reflect habitation of 500-2,000-m depths and likely reflect morphologies seen in zoarcids living on continental slopes elsewhere in the world. This balance among the sensory modalities makes zoarcids relatively generalized among secondary deep-sea fishes and may be one of the reasons this opportunistic and adaptable group has been successful in colonizing a variety of emergent and ephemeral habitats.

Brain and sense organ anatomy and histology in hemoglobinless Antarctic icefishes (Perciformes: Notothenioidei: Channichthyidae).

The Channichthyidae, one of five Antarctic notothenioid families, includes 16 species and 11 genera. Most live at depths of 200-800 m and are a major component of fish biomass in many shelf areas. Channichthyids are unique among adult fishes in possessing pale white blood containing a few vestigal erythrocytes and no hemoglobin. Here we describe the brains of seven species and special sense organs of eight species of channichthyids. We emphasize Chionodraco hamatus and C. myersi, compare these species to other channichthyids, and relate our findings to what is known about brains and sense organs of red-blooded notothenioids living sympatrically on the Antarctic shelf. Brains of channichthyids generally resemble those of their bathydraconid sister group. Among channichthyids the telencephalon is slightly regressed, resulting in a stalked appearance, but the tectum, corpus cerebellum, and mechanoreceptive areas are well developed. Interspecific variation is present but slight. The most interesting features of channichthyid brains are not in the nervous tissue but in support structures: the vasculature and the subependymal expansions show considerable elaboration. Channichthyids have large accessory nasal sacs and olfactory lamellae are more numerous than in other notothenioids. The eyes are relatively large and laterally oriented with similar duplex (cone and rod) retinae in all eight species. Twin cones are the qualitatively dominant photoreceptor in histological sections and, unlike bathydraconids, there are no species with rod-dominated retinae. Eyes possess the most extensive system of hyaloid arteries known in teleosts. Unlike the radial pattern seen in red-blooded notothenioids and most other teleosts, channichthyid hyaloid arteries arise from four or five main branches and form a closely spaced anastomosing series of parallel channels. Cephalic lateral line canals are membranous and some exhibit extensions (canaliculi), but canals are more ossified than those of deeper-living bathydraconids. We conclude that, with respect to the anatomy and histology of the neural structures, the brain and sensory systems show little that is remarkable compared to other fishes, and exhibit little diversification within the family. Thus, the unusual habitat and a potentially deleterious mutation resulting in a hemoglobinless phenotype are reflected primarily in expansion of the vasculature in the brain and eye partially compensating for the absence of respiratory pigments. Neural morphology gives the impression that channichthyids are a homogeneous and little diversified group.

Diversification of brain and sense organ morphology in Antarctic dragonfishes (Perciformes: Notothenioidei: Bathydraconidae).

In the subzero shelf waters of Antarctica, fishes of the perciform suborder Notothenioidei dominate the fish fauna and constitute an adaptive radiation and a species flock. The 16 species of dragonfishes of the family Bathydraconidae live from surface waters to nearly 3,000 m and have the greatest overall depth range among notothenioid families. We examined the anatomy and histology of the brain, retina, and cephalic lateral line system of nine bathydraconid species representing 8 of the 11 known genera. We evaluate these data against a cladogram identifying three clades in the family. We provide a detailed drawing of the brain and cranial nerves of Gymnodraco acuticeps and Akarotaxis nudiceps. Bathydraconid brain morphology falls into two categories. Brains of most species are similar to those of generalized perciforms and some basal notothenioids (Class I). However, brains of deep-living bathydraconids (members of the tribe Bathydraconini minus Prionodraco) have a reduced telencephalon and tectum that renders the neural axis visible - the stalked brain morphology (Class II). All bathydraconids have duplex (rod and cone) retinae but there is considerable interspecific variation in the ratio of cones:rods and in the number of cells in the internal nuclear layer. Retinal histology reflects habitat depth but is not tightly coupled to phylogeny. Although the deep-living species of Bathydraconini have rod-dominated retinae, the retinae of some sister species are photopic. An expanded cephalic lateral line system is also characteristic of all members of the Bathydraconini as exemplified by Akarotaxis. This morphology includes large lateral line pores, wide membranous canals, hypertrophied canal neuromasts, and large anterodorsal lateral line nerves, eminentia granulares, and crista cerebellares. The saccular otoliths are also enlarged in members of this tribe. Neural diversification among bathydraconids on the Antarctic shelf has not involved the evolution of sensory specialists. Brain and sense organ morphologies do not approach the specialized condition seen in primary deep-sea fishes or even that of some secondary deep-sea fishes including sympatric non-notothenioids such as liparids (snailfishes) and muraenolepidids (eel cods). The brains and sense organs of bathydraconids, including the deep-living species, reflect their heritage as perciform shorefishes.

Anatomy and histology of the brain and sense organs of the antarctic plunderfish Dolloidraco longedorsalis (Perciformes: Notothenioidei: Artedidraconidae), with comments on the brain morphology of other artedidraconids and closely related harpagiferids.

In the high-latitude shelf waters of Antarctica, fishes in the perciform suborder Notothenioidei dominate the fish fauna and constitute an adaptive radiation and a species flock. The 25 species of notothenioid plunderfishes, comprising four genera of the family Artedidraconidae, contribute substantially to fish species diversity on the high Antarctic shelf. A mental barbel is an autapomorphy for the family. Dolloidraco longedorsalis is the most abundant artedidraconid at depths over 400 m in these waters. In this article we present the anatomy and histology of the brain and special sense organs of Dolloidraco and compare it to the brains of other artedidraconids, closely related harpagiferids, and more generally to other notothenioids. We provide a detailed drawing of the brain and cranial nerves. The brain of Dolloidraco is simple, without external hypertrophy of sensory or motor regions, but contains several unusual features associated with the ventricular system and CSF, including well-developed circumventricular organs, subependymal expansions, and subarachnoid cisterns; and a ventricle in the corpus cerebellum. The brain of Dolloidraco also contains a lobed chief sensory nucleus of the trigeminal nerve that is correlated across species with barbel length. The eyes are large and contain a small choroid rete, a structure previously thought to be absent from members of this family. We document the histology of the duplex retina, olfactory apparatus, cutaneous taste buds, and barbel musculature and innervation. We discuss the role of pedomorphy in producing simplified brain morphologies. We consider the possibility that Dolloidraco is a somatosensory specialist-an unusual feature among vertebrates-and decide that this is unlikely.

TESTING HYPOTHESES OF NEURAL EVOLUTION IN GYMNOTIFORM ELECTRIC FISHES USING PHYLOGENETIC CHARACTER DATA.

In this paper, we propose a method to test alternative hypotheses of phenotypic evolution. The method compares patterns observed in phylogenetic character data with patterns expected by explicit models of evolutionary process. Observed patterns of character-state diversity are assessed from four properties of character-state change derived from a phylogenetic analysis: the sequence and correlation of transformations on a cladogram and the spatial and functional localization of these transformations to parts of an organism. Patterns expressed in terms of the localization of transformations are compared with the expectations of null models that the number of transformations is proportional to measures of size or complexity. Deviations from the values expected by the null models are then compared with qualitative expectations of the models. The method is applied to characters in the nervous system of gymnotiform electric fishes. Patterns in the diversity of 63 reconstructed character-state changes are compared with the expectations of 10 published models of neural evolution. A total of 63 expectations are reviewed, of which 33 (52%) are found to be consistent with the gymnotiform neural data. In general, the models reviewed are not successful at making global predictions, in part because they have been cast in excessively general terms. The data support the conclusion that evolution in the nervous system of gymnotiforms has involved a mosaic of processes, each operating differentially on functional and developmental systems and at different spatial and temporal scales. The results also indicate that more refined models are required, each making more explicit predictions.

Patterns and processes of brain diversification within esociform teleosts.

The richness of nervous systems represented by extant fishes has not yet been fully determined; the brain morphology of many groups remains undescribed. For this reason we have begun to examine the brains of esociforms, a group representing basal euteleosts, focusing here on three goals: 1) to provide the first general descriptions of the brains of two esociform teleosts, Esox masquinongy (muskellunges) and Esox lucius (northern pikes); 2) to describe the neuronal development of E. masquinongy; and 3) to compare the differences in neuronal features between E. masquinongy and E. lucius with reference to the ontogeny of E. masquinongy. We demonstrate that relative to the brains of E. lucius and other basal euteleosts, the brains of E. masquinongy exhibit several paedomorphic features involving the position and morphology of nuclei present throughout the brain. This heterochronic shift parallels differences in nonneural morphological features described between these two species. We conclude that at finer taxonomic levels in some groups such as esocids, aspects of neuronal diversification may be explained by evolutionary transformations involving all body systems. © 1996 Wiley-Liss, Inc.

Lateral-line neuromast development in Ambystoma mexicanum and a comparison with Rana pipiens.

We have examined the embryonic development of the major neuromast lines of the lateral-line system in the urodele Ambystoma mexicanum both in vivo (using microsurgical techniques to transplant placodes) and in preserved embryos using scanning electron microscopy (SEM). We have compared this to SEM observations of embryos of the anuran Rana pipiens. We have determined the approximate locations of the lateral-line placodes in A. mexicanum and the approximate timing of both the migration of the lateral line primordia and the neuromast eruption in both species. We find that, at hatching, all primary neuromasts are present and fully formed in Ambystoma, while migration of the primordia is just beginning in Rana. The neuromast systems in both species are fully formed by the time feeding begins. If neuromast eruption is considered in relation to developmental events other than hatching, fewer differences are found between species, suggesting that hatching is precocious in Rana. We find no evidence of heterochrony to account for the morphological differences observed in these lateral-line systems. Orthogonal neuromasts on the head, a derived feature of urodeles, appears to be the result of lateral neuromast movement subsequent to the rostral migration of the primordia. This process was not observed in the anuran. In addition, we observe that ciliated epidermal cells disappear from the area immediately around each of the lines and suggest that neuromasts cause the regression of cilia in their immediate vicinity.

Neuromast topography in anuran amphibians.

Generalized anuran tadpoles across families exhibit a similar neuromast morphology on their heads, as follows: (1) all neuromast lines known for anurans are present; (2) within these lines total neuromast number ranges from about 250 to 320; (3) neuromasts form linear stitches composed of two to three, but sometimes up to five, neuromasts; (4) neuromast linear dimensions are ⩽ 10 µm; and (5) neuromasts contain ⩽ 15 hair cells. Compared with generalized forms, stream, arboreal, carnivorous, and desert-pond forms have fewer neuromasts but they contain more hair cells. They do not, however, form stitches. Obligate midwater suspension-feeding forms, including Xenopus (Pipidae), Rhinophrynus (Rhinophyrnidae), and Phrynomerus (Microhylidae), form stitches that contain > six, but potentially up to 18 or more, loosely aggregated neuromasts. Xenopus and Rhinophrynus have large neuromasts (up to 40 µm across). Chiasmocleis (Microhylidae) tadpoles form stiches that are linearly arranged with up to ten neuromasts. Whereas urodeles can have more than one neuromast row per line and may form both linear and transverse stitches, anurans have only one row of neuromasts per line and form only transverse stitches. Neuromasts in anurans tend to be smaller and more circular than in urodeles and positioned flush with the epidermal surface. A greater percentage of anurans form stitches, and anurans have greater intrafamilial variation in stitch formation than do urodeles.

Neuromast topography in urodele amphibians.

Using scanning electron microscopy I determined neuromast number and orientation, neuromast sensory epithelial surface area and relative position, hair cell number per neuromast, hair cell size, and stitch formation in aquatic urodeles. All aquatic salamanders examined (34 specimens, 20 species, 16 genera, nine families) had neuromasts. The basic pattern of neuromast organization was similar in all species, consisting of a single row of circumorbital (supraorbital + infraorbital) neuromasts and anteriorly along the snout two rows of nasal and three rows of maxillary neuromasts. Nasal and maxillary groups consisted of orthogonally oriented neuromasts. Variation in most parameters occured at every taxonomic level, between individuals of the same species, and even on opposite sides of the same individual. Among species, primary neuromast number ranged from 94 to 150, with plethodontids having higher numbers. Despite high intraspecific variation, neuromast number fell into a sufficiently narrow range to be useful systematically. Hair cell number per neuromast was greater in species with larger animals. Hair cell number per neuromast and number of primary neuromasts did not increase with growth. In some species primary neuromasts divided to form secondary neuromasts (together termed a stitch). Two types of stitches-transverse and longitudinal-were formed. Transverse stitches were characteristic of ambystomatids and cryptobranchids, longitudinal stitches were characteristic of proteids and salamandrids. Because transverse stitches are also characteristic of anurans, this trait may be the generalized condition in at least these two amphibian orders. With stitch formation total number of hair cells on the dorsal surface of the head of these animals can be increased over tenfold to almost 20,000. Ecologically, lentic forms tended to form transverse stitches, while lotic forms had single neuromasts in epidermal pits or longitudinal stitches in epidermal grooves. Lotic forms also tended to have more primary neuromasts and more nasal and maxillary neuromasts.