Biochemical adaptations of notothenioid fishes: comparisons between cold temperate South American and New Zealand species and Antarctic species

Fishes of the perciform suborder Notothenioidei afford an excellent opportunity for studying the evolution and functional importance of diverse types of biochemical adaptation to temperature. Antarctic notothenioids have evolved numerous biochemical adaptations to stably cold waters, including antifreeze glycoproteins, which inhibit growth of ice crystals, and enzymatic proteins with cold-adapted specific activities (k(cat) values) and substrate binding abilities (K(m) values), which support metabolism at low temperatures. Antarctic notothenioids also exhibit the loss of certain biochemical traits that are ubiquitous in other fishes, including the heat-shock response (HSR) and, in members of the family Channichthyidae, hemoglobins and myoglobins. Tolerance of warm temperatures is also truncated in stenothermal Antarctic notothenioids. In contrast to Antarctic notothenioids, notothenioid species found in South American and New Zealand waters have biochemistries more reflective of cold-temperate environments. Some of the contemporary non-Antarctic notothenioids likely derive from ancestral species that evolved in the Antarctic and later "escaped" to lower latitude waters when the Antarctic Polar Front temporarily shifted northward during the late Miocene. Studies of cold-temperate notothenioids may enable the timing of critical events in the evolution of Antarctic notothenioids to be determined, notably the chronology of acquisition and amplification of antifreeze glycoprotein genes and the loss of the HSR. Genomic studies may reveal how the gene regulatory networks involved in acclimation to temperature differ between stenotherms like the Antarctic notothenioids and more eurythermal species like cold-temperate notothenioids. Comparative studies of Antarctic and cold-temperate notothenioids thus have high promise for revealing the mechanisms by which temperature-adaptive biochemical traits are acquired - or through which traits that cease to be of advantage under conditions of stable, near-freezing temperatures are lost - during evolution.     

Buoyancy of sub-Antarctic notothenioids including the sister lineage of all other notothenioids (Bovichtidae)

The radiation of notothenioid fishes (Perciformes) in Antarctic waters was likely the result of an absence of competition in the isolated Antarctic waters and key traits such as the production of antifreeze glycoprotein and buoyancy modifications. Although notothenioids lack a swim bladder, the buoyancy of Antarctic species, ranging from neutrally buoyant to relatively heavy, corresponds to diverse life styles. The buoyancy of South American notothenioids has not been studied. Static buoyancy was measured in adult notothenioids (n = 263, from six species of the sub-order Notothenioidei, families Bovichtidae, Eleginopidae, Nototheniidae, and Harpagiferidae) from the Beagle Channel. Measurements were expressed as percentage buoyancy (%B). Buoyancy ranged from 3.88 to 6.96% (median, 4.0–6.7%), and therefore, all species could be considered benthic consistent with previous studies that found that neutral buoyancy in notothenioids is rare. Harpagifer bispinis, Patagonotothen cornucola, and Cottoperca gobio were significantly less buoyant than Paranotothenia magellanica. The buoyancy values of most species were concordant with known habitat preferences. These data, especially the data of C. gobio (sister lineage of all other nototehnioids) and E. maclovinus (sister lineage of the Antarctic clade of notothenioids), could be useful for understanding the diversification of this feature during the notothenioid radiation.     

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.     

Karyotype and genome size of zoarcids and notothenioids (Taleostei,Perciformes) from the Ross Sea: cytotaxonomic implications

In the absence of fossils, the origin of Notothenioidei, a perciform suborder dominating the fish fauna of the Southern Ocean, remains conjectural; some morphoecological evidence suggests relationships to zoarcoids. To test this point we have compared the karyotype morphology and genome size of two species of zoarcids from the Ross Sea to those of one species each of the notothenioid families Artedidraconidae, Bathydraconidae, Channichthyidae and Nototheniidae from the same region. A karyotype of 48, mostly acrocentric, chromosomes, localization of nucleolar organizers on a pair of small dibrachial chromosomes, a genome size of about 3 pg of DNA, characterize both zoarcids; similar features can be found in the karyology of the notothenioids (especially the Nototheniidae). However, all shared characters appear as plesiomorphic in teleost karyology, which does not help in producing new data on the problem of notothenioid relationships.     

Phylogenetic investigations of Antarctic notothenioid fishes (Perciformes: Notothenioidei) using complete gene sequences of the mitochondrial encoded 16S rRNA

The Notothenioidei dominates the fish fauna of the Antarctic in both biomass and diversity. This clade exhibits adaptations related to metabolic function and freezing avoidance in the subzero Antarctic waters, and is characterized by a high degree of morphological and ecological diversity. Investigating the macroevolutionary processes that may have contributed to the radiation of notothenioid fishes requires a well-resolved phylogenetic hypothesis. To date published molecular and morphological hypotheses of notothenioids are largely congruent, however, there are some areas of significant disagreement regarding higher-level relationships. Also, there are critical areas of the notothenioid phylogeny that are unresolved in both molecular and morphological phylogenetic analyses. Previous molecular phylogenetic analyses of notothenioids using partial mtDNA 12S and 16S rRNA sequence data have resulted in limited phylogenetic resolution and relatively low node support. One particularly controversial result from these analyses is the paraphyly of the Nototheniidae, the most diverse family in the Notothenioidei. It is unclear if the phylogenetic results from the 12S and 16S partial gene sequence dataset are due to limited character sampling, or if they reflect patterns of evolutionary diversification in notothenioids. We sequenced the complete mtDNA 16S rRNA gene for 43 notothenioid species, the largest sampling to-date from all eight taxonomically recognized families. Phylogenetic analyses using both maximum parsimony and maximum likelihood resulted in well-resolved trees with most nodes supported with high bootstrap pseudoreplicate scores and significant Bayesian posterior probabilities. In all analyses the Nototheniidae was monophyletic. Shimodaira–Hasegawa tests were able to reject two hypotheses that resulted from prior morphological analyses. However, despite substantial resolution and node support in the 16S rRNA trees, several phylogenetic hypotheses among closely related species and clades were not rejected. The inability to reject particular hypotheses among species in apical clades is likely due to the lower rate of nucleotide substitution in mtDNA rRNA genes relative to protein coding regions. Nevertheless, with the most extensive notothenioid taxon sampling to date, and the much greater phylogenetic resolution offered by the complete 16S rRNA sequences over the commonly used partial 12S and 16S gene dataset, it would be advantageous for future molecular investigations of notothenioid phylogenetics to utilize at the minimum the complete gene 16S rRNA dataset.     

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.     

Diversification of brain morphology in antarctic notothenioid fishes: Basic descriptions and ecological considerations

The Notothenioidei, a perciform suborder of 120 species, dominates the ichthyofauna of the Southern Ocean around Antarctica. Unlike most teleost groups, notothenioids have undergone a corresponding ecological and phyletic diversification and therefore provide an excellent opportunity to study the divergence of the nervous system in an unusual environment. Our goal is to evaluate notothenioid brain variation in light of this diversification. To provide a baseline morphology, we examine the gross morphology and histology of the brain of Trematomus bernacchii, a generalized member of the family Nototheniidae. We then examine the variation in brain gross anatomy (32 species) and histology (10 species) of other notothenioids. Our sample represents about 27% of the species in this group and includes species from each of the six families, as well as species representing diverse ecologies. For comparison we reference the well-studied brains of two species of temperate perciformes (Perca flavescens and Lepomis humilis). Our results show that, in general, notothenioid brains are more similar to the brains of temperate perciforms than to the unusual brains of cave-dwelling and deep-sea fishes. Interspecific variation in gross brain morphology is comparable to that in Old World cyprinids and is illustrated for 17 species. Variation is especially noteworthy in the ecologically and geographically diverse family Nototheniidae. Measurements indicate that sensory regions (olfactory bulbs, eminentia granularis, and crista cerebellaris) exhibit the most pronounced variation in relative surface area. Association areas, including the corpus cerebelli and the telencephalon, exhibit moderate variation in size, shape, and lobation patterns. Regulatory areas of the brain, including the saccus vasculosus and the subependyma of the third ventricle, are also variable. These regions are best developed in species living in the subfreezing water close to the continent. In some species the expanded ependymal lining forms ventricular sacs, not previously described in any other vertebrate. Three species, including two nototheniids (Eleginops maclovinus and Pleuragramma antarcticum) and the only artedidraconid in our sample, have distinctive brains. The unique brain morphology of Pleuragramma is probably related to a sensory (lateral line) specialization for feeding. Within the Nototheniidae, a phyletic effect on cerebellar morphology is evident in the Coriiceps group and in the Pleuragramminae. Neither phyletic position nor ecological factors (water temperature, position in the water column, dietary habits) alone fully expalin the pattern of notothenioid brain diversification. © 1995 Wiley-Liss, Inc.     

Some like it hot, some like it cold: the heat shock response is found in New Zealand but not Antarctic notothenioid fishes

Previous research on Antarctic notothenioids has demonstrated that cells of cold-adapted Antarctic notothenioids lack a common cellular defense mechanism called the heat shock response (HSR), the induction of a family of heat shock proteins (Hsps) in response to elevated temperatures. The goal of this study was to address how widespread the loss of the HSR is within the Notothenioidei suborder and, specifically, to ask whether cold temperate non-Antarctic notothenioids possess the HSR. In general, Antarctic fish have provided an important opportunity for physiologists to examine responses to selection in the environment and to ask whether traits of the notothenioids represent cold adaptation, or whether the traits are related to history and are characteristics of the notothenioid lineage. Using in vivo metabolic labeling, results indicate that one of the two New Zealand notothenioids possess an HSR. The thornfish, Bovichtus variegatus Richardson, 1846, expressed heat shock proteins (Hsp) in response to heat stress, whereas the black cod, Notothenia angustata Hutton, 1875, did not display robust stress-inducible Hsp synthesis at the protein-level. However, further analysis using Northern blotting clearly demonstrated that mRNA for a common Hsp gene, hsp70, was present in cells of both New Zealand species following exposure to elevated temperatures. Overall, combined evidence on the HSR in notothenioid fishes from temperate New Zealand waters indicate that the loss of the HSR in Antarctic notothenioid fishes occurred after the separation of Bovichtidae from the other Antarctic notothenioid families, and that the HSR was most likely lost during evolution at cold and constant environmental temperatures.     

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.     

The nature of the diversity of Antarctic fishes

The species diversity of the Antarctic fish fauna changed notably during the 40 million years from the Eocene to the present. A taxonomically restricted and endemic modern fauna succeeded a taxonomically diverse and cosmopolitan Eocene fauna. Although the Southern Ocean is 10% of the worlds ocean, its current fish fauna consists of only 322 species, small considering the global diversity of 25,000–28,000 species. The fauna is reasonably well-known from a taxonomic perspective. This intermediate designation between poorly known and well-known indicates that new species are regularly being described. A conservative estimate of the number of undescribed species is 30–60; many of these may be liparids. On the Antarctic continental shelf and upper slope the fauna includes 222 species from 19 families of benthic fishes. The most speciose taxa are notothenioids, liparids and zoarcids, accounting for 88% of species diversity. Endemism for Antarctic species is also, coincidentally, 88%, at least threefold higher than in faunas from other isolated marine localities. Eight notothenioid families, including five that are primarily Antarctic, encompass a total of 44 genera and 129 species, 101 Antarctic and 28 non-Antarctic. The 101 Antarctic species make up 45% of the benthic species diversity in the Antarctic region. However, at the highest latitudes, notothenioids contribute 77% of the species diversity, 92% of the abundance and 91% of the biomass. Although species diversity is low compared to other shelf habitats, the nature of the adaptive radiation in organismal diversity among notothenioids is noteworthy in the marine realm. In some notothenioid clades phyletic diversification was accompanied by considerable morphological and ecological diversification. The exemplar is the benthic family Nototheniidae that underwent a habitat or depth related diversification centred on the alteration of buoyancy. They occupy an array of pelagic and benthopelagic habitats at various depths on the shelf and upper slope. Diversification in buoyancy is the hallmark of the nototheniid radiation and, in the absence of swim bladders, was accomplished by a combination of reduced skeletal mineralisation and lipid deposition. Although neutral buoyancy is found in only five species of nototheniids some, like Pleuragramma antarcticum, are abundant and ecologically important. Much work remains to be done in order to frame and to use phylogenetically based statistical methods to test hypotheses relating to the key features of the notothenioid radiation. To reach this analytical phase more completely resolved cladograms that include phyletically basal and non-Antarctic species are essential.     

Antarctic Crabs: Invasion or Endurance?

Recent scientific interest following the “discovery” of lithodid crabs around Antarctica has centred on a hypothesis that these crabs might be poised to invade the Antarctic shelf if the recent warming trend continues, potentially decimating its native fauna. This “invasion hypothesis” suggests that decapod crabs were driven out of Antarctica 40–15 million years ago and are only now returning as “warm” enough habitats become available. The hypothesis is based on a geographically and spatially poor fossil record of a different group of crabs (Brachyura), and examination of relatively few Recent lithodid samples from the Antarctic slope. In this paper, we examine the existing lithodid fossil record and present the distribution and biogeographic patterns derived from over 16,000 records of Recent Southern Hemisphere crabs and lobsters. Globally, the lithodid fossil record consists of only two known specimens, neither of which comes from the Antarctic. Recent records show that 22 species of crabs and lobsters have been reported from the Southern Ocean, with 12 species found south of 60°S. All are restricted to waters warmer than 0°C, with their Antarctic distribution limited to the areas of seafloor dominated by Circumpolar Deep Water (CDW). Currently, CDW extends further and shallower onto the West Antarctic shelf than the known distribution ranges of most lithodid species examined. Geological evidence suggests that West Antarctic shelf could have been available for colonisation during the last 9,000 years. Distribution patterns, species richness, and levels of endemism all suggest that, rather than becoming extinct and recently re-invading from outside Antarctica, the lithodid crabs have likely persisted, and even radiated, on or near to Antarctic slope. We conclude there is no evidence for a modern-day “crab invasion”. We recommend a repeated targeted lithodid sampling program along the West Antarctic shelf to fully test the validity of the “invasion hypothesis”.     

Cytogenetic mapping of immunoglobulin heavy chain genes in Antarctic fish

The chromosomal location of the IgH locus has been analyzed in several bony fish of the Antarctic perciform group Notothenioidei. Two IgH probes were prepared from the species Trematomus bernacchii (family Nototheniidae, tribe Trematominae) and mapped onto the chromosomes of ten species belonging to the same genus (Trematomus) and in two outgroups, through one-color and two-color FISH. A single location of the IgH locus was found in the majority of the species examined, including the outgroups, whereas in four of them the IgH genes splited to two chromosomal loci. RT-PCR experiments revealed the presence of three allelic sequences in T. newnesi, a species in which the IgH genes were organized in two chromosomal loci. Possible pathways leading to IgH genes duplication during the diversification of trematomine fishes were inferred from the analysis of the FISH patterns in a phylogenetic context. The present work provides the first comprehensive picture of IgH genes organization at chromosomal level in a bony fish group.     

Comparative population genetics of seven notothenioid fish species reveals high levels of gene flow along ocean currents in the southern Scotia Arc, Antarctica

The Antarctic fish fauna is characterized by high endemism and low species diversity with one perciform suborder, the Notothenioidei, dominating the whole species assemblage on the shelves and slopes. Notothenioids diversified in situ through adaptive radiation and show a variety of life history strategies as adults ranging from benthic to pelagic modes. Their larval development is unusually long, lasting from a few months to more than a year, and generally includes a pelagic larval stage. Therefore, the advection of eggs and larvae with ocean currents is a key factor modulating population connectivity. Here, we compare the genetic population structures and gene flow of seven ecologically distinct notothenioid species of the southern Scotia Arc based on nuclear microsatellites and mitochondrial DNA sequences (D-loop/cytochrome b). The seven species belong to the families Nototheniidae (Gobionotothen gibberifrons, Lepidonotothen squamifrons, Trematomus eulepidotus, T. newnesi) and Channichthyidae (Chaenocephalus aceratus, Champsocephalus gunnari, Chionodraco rastrospinosus). Our results show low-population differentiation and high gene flow for all investigated species independent of their adult life history strategies. In addition, gene flow is primarily in congruence with the prevailing ocean current system, highlighting the role of larval dispersal in population structuring of notothenioids.     

The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review

The Ross Sea, a large, high-latitude (72–78°S) embayment of the Antarctic continental shelf, averages 500 m deep, with troughs to 1,200 m and the shelf break at 700 m. It is covered by pack ice for 9 months of the year. The fish fauna of about 80 species includes primarily 4 families and 53 species of the endemic perciform suborder Notothenioidei. This review focuses on the diet and role in the food web of notothenioids and top-level bird and mammal predators, and also includes new information on the diets of artedidraconids and bathydraconids. Although principally a benthic group, notothenioids have diversified to form an adaptive radiation that includes pelagic and semipelagic species. In the southern Ross Sea, notothenioids dominate the fish fauna at levels of abundance and biomass >90% and are, therefore, inordinately important in the food web. Antarctic krill (Euphausia superba) and mesopelagic fishes are virtually absent from the shelf waters of the Ross Sea. Of the four notothenioid families, nototheniids show the most ecological and dietary diversification, with pelagic, cryopelagic, epibenthic and benthic species. Neutrally buoyant Pleuragramma antarcticum constitutes >90% of both the abundance and biomass of the midwater fish fauna. Most benthic nototheniids are opportunistic and feed on seasonally or locally abundant zooplanktonic prey. Artedidraconids are benthic sit-and-wait predators. Larger bathydraconids are benthic predators on fish while smaller species feed mainly on benthic crustaceans. Channichthyids are less dependent on the bottom for food than other notothenioids. Some species combine benthic and pelagic life styles; others are predominantly pelagic and all consume euphausiids and/or fish. South polar skuas, Antarctic petrels, Adélie and emperor penguins, Weddell seals and minke and killer whales are the higher vertebrate components of the food web, and all prey on notothenioids to some extent. Based on the frequency of occurrence of prey items in the stomachs of fish, bird and mammal predators, P. antarcticum and ice krill E. crystallorophias are the key species in the food web of the Ross Sea. P. antarcticum is a component of the diet of at least 11 species of nototheniid, bathydraconid and channichthyid fish and, at frequencies of occurrence from 71 to 100%, is especially important for Dissostichus mawsoni, Gvozdarus svetovidovi and some channichthyids. At least 16 species of notothenioids serve as prey for bird and mammal predators, but P. antarcticum is the most important and is a major component of the diet of south polar skua, Adélie and emperor penguins and Weddell seals, at frequencies of occurrence from 26 to 100%. E. crystallorophias is consumed by some nototheniid and channichthyid fish and can be of importance in the diet of emperor and Adélie penguins, although in the latter case, this is dependent on location and time of year.Unlike the linear phytoplanktonE. superbaconsumers of the E. superba food chain hypothesized for much of the Southern Ocean, the food web of the Ross Sea shelf is non-linear, with complex prey-predator interactions. Notothenioid fish play a key role: as predators, they occupy most of the trophic niches available in the ecosystem, relying on benthic, zooplanktonic and nektonic organisms; as prey, they are important food resources for each other and for most top predators living and foraging on the shelf. They also constitute the major link between lower (invertebrates) and higher (birds and mammals) levels of the food web. This is especially true for P. antarcticum. Along with E. crystallorophias, its ecological role in the Ross Sea is equivalent to that of myctophids and E. superba elsewhere in the Southern Ocean.     

Renal glomerular evolution in Antarctic notothenioid fishes

Light and electron microscopy were used to document the degree of glomerular development in 10 species of Antarctic notothenioid fishes. When combined with results of previous studies, data revealed that 16 of 20 species inhabiting subzero sea water were aglomerular. One subantarctic and two temperate species were pauciglomerular, and an additional temperate species had a moderate number of glomeruli. Renal corpuscles were variable in number and diameter among the pauciglomerular species, and most had few patent glomerular capillaries. Radiolabelled markers indicated that the glomerular filtration rate was low in the pauciglomerular Notothenia angustata , ranging from 0.005 to 0.124 ml h⁻¹ kg⁻¹ in eight specimens. Arterial perfusion of Microfil demonstrated that arteries supplying aglomerular and pauciglomerular kidneys were confined largely to the periphery of the organ, and glomerular capillaries were absent or few in number. As ancestral notothenioids probably had glomerular kidneys, data from 20–25% of the fauna suggest that there has been an evolutionary loss of glomeruli in many species. The pattern of glomerular reduction is consistent with the hypothesis that the selective advantage of aglomerularism is in the urinary conservation of small molecular weight antifreeze glycopeptide compounds that are vital to survival in sub-zero Antarctic waters.     

The evolution of polar fish hemoglobin: a phylogenetic analysis of the ancestral amino acid residues linked to the root effect

Originating from a benthic ancestor, the suborder Notothenioidei (the dominant fish fauna component of the Antarctic sea) underwent a remarkable radiation, which led notothenioids to fill several niches. The ecological importance of notothenioids in Antarctica and their biochemical adaptations have prompted great efforts to study their physiology and phylogeny, with special attention to the evolutionary adaptation of the oxygen-transport system. We herewith report the evolutionary history of alpha- and beta-globins under the assumption of the molecular clock hypothesis as a basis for reconstructing the phylogenetic relationships among species. These studies have been extended to fish species of other latitudes, including the Arctic region. The northern and southern polar oceans have very different characteristics; indeed, in many respects the Antarctic and Arctic ichthyofaunas are more dissimilar than similar. Our results show that the inferred phylogeny of Arctic and Antarctic globins is different. Taking advantage of the wealth of information collected on structure and function of hemoglobins, we have attempted to investigate the evolutionary history of an important physiological feature in fish, the Root effect. The results suggest that the amino acid residues reported to play a key role in the Root effect may be regarded as ancestor characters, but the lack of this effect in extant species can hardly be associated with the presence of synapomorphies.     

On the origin and trigger of the notothenioid adaptive radiation

Adaptive radiation is usually triggered by ecological opportunity, arising through (i) the colonization of a new habitat by its progenitor; (ii) the extinction of competitors; or (iii) the emergence of an evolutionary key innovation in the ancestral lineage. Support for the key innovation hypothesis is scarce, however, even in textbook examples of adaptive radiation. Antifreeze glycoproteins (AFGPs) have been proposed as putative key innovation for the adaptive radiation of notothenioid fishes in the ice-cold waters of Antarctica. A crucial prerequisite for this assumption is the concurrence of the notothenioid radiation with the onset of Antarctic sea ice conditions. Here, we use a fossil-calibrated multi-marker phylogeny of nothothenioid and related acanthomorph fishes to date AFGP emergence and the notothenioid radiation. All time-constraints are cross-validated to assess their reliability resulting in six powerful calibration points. We find that the notothenioid radiation began near the Oligocene-Miocene transition, which coincides with the increasing presence of Antarctic sea ice. Divergence dates of notothenioids are thus consistent with the key innovation hypothesis of AFGP. Early notothenioid divergences are furthermore congruent with vicariant speciation and the breakup of Gondwana.     

南极鱼类多样性和适应性进化研究进展

南极地区是地球上唯一未被人类活动大量影响的地区, 其极端寒冷的环境为南极生物的进化提供了“温床”。过去三千万年间, 南极鱼亚目鱼类在南极海洋逐渐变冷的过程中快速进化, 从一个温暖海域的底栖祖先分化成南极海域最为多样化的鱼类类群。由于其在南极圈内和南极圈外的各种温度区间都有分布, 因而成为研究鱼类适应性进化和耐寒机制的良好生物模型。本文综述了有关南极海域鱼类区系组成与物种多样性现状, 南极鱼亚目鱼类适应低温的一系列特化的生物学性状及其关键的遗传进化机制。现有研究表明: 南极鱼类在几千万年零度以下低温环境的进化中发生了大量基因的大规模扩增和基因表达的改变, 如铁调素、卵壳蛋白和逆转座子等118个基因发生了显著的扩增。另外, 有些从南极鱼中获得的抗寒基因已经用于提高动植物低温抗性的研究并取得了良好的效果。在今后的几年中, 将会有多个南极鱼物种的全基因组得到破译, 在低温适应相关基因的功能和进化方面的研究也会更加深入, 这些研究将深入揭示低温压力下基因组的进化规律以及鱼类低温适应的分子机制。