Experimental evidence for trait utility of gill raker number in adaptive radiation of a north temperate fish

North temperate fish in post‐glacial lakes are textbook examples for rapid parallel adaptive radiation into multiple trophic specialists within individual lakes. Speciation repeatedly proceeded along the benthic–limnetic habitat axis, and benthic–limnetic sister species diverge in the number of gill rakers. Yet, the utility of different numbers of gill rakers for consuming benthic vs. limnetic food has only very rarely been experimentally demonstrated. We bred and raised families of a benthic–limnetic species pair of whitefish under common garden conditions to test whether these species (i) show heritable differentiation in feeding efficiency on zooplankton, and (ii) whether variation in feeding efficiency is predicted by variation in gill raker numbers. We used zooplankton of three different size classes to investigate prey size dependency of divergence in feeding efficiency and to investigate the effect strength of variation in the number of gill rakers. Our results show strong interspecific differences in feeding efficiency. These differences are largest when fish were tested with the smallest zooplankton. Importantly, feeding efficiency is significantly positively correlated with the number of gill rakers when using small zooplankton, also when species identity is statistically controlled for. Our results support the hypothesis that a larger number of gill rakers are of adaptive significance for feeding on zooplankton and provide one of the first experimental demonstrations of trait utility of gill raker number when fish feed on zooplankton. These results are consistent with the suggested importance of divergent selection driven feeding adaptation during adaptive radiation of fish in post‐glacial lakes.     

Genetic differentiation in gill raker number and length in sympatric anadromous and nonanadromous morphs of sockeye salmon, Oncorhynchus nerka

The genetic and environmental basis for polymorphism in gill raker number and length in sympatric anadromous and nonanadromous morphs of sockeye salmon, Oncorhynchus nerka, was investigated. Analysis of 30 full sib families involving pure types and reciprocal hybrids revealed that the variation was partitioned significantly among families within cross types and among cross types in both traits. As in the wild, kokanee displayed more gill rakers than sockeye; reciprocal hybrids displayed intermediate counts. Gill raker length also varied markedly among cross types, with pure sockeye displaying 19% longer gill rakers than comparable sized kokanee. This difference was in the opposite direction predicted, given the common positive association between gill raker number and length in sympatric morphs of the same species in fishes. Gill raker number and length were generally not correlated within cross types, suggesting independent divergence of the traits. The results are discussed in relation to genetic and trophic divergence of the morphs and to factors selecting for differentiation in the two gill raker traits.     

Diversifying selection drives parallel evolution of gill raker number and body size along the speciation continuum of European whitefish

Adaptive radiation is the evolution of ecological and phenotypical diversity. It arises via ecological opportunity that promotes the exploration of underutilized or novel niches mediating specialization and reproductive isolation. The assumed precondition for rapid local adaptation is diversifying natural selection, but random genetic drift could also be a major driver of this process. We used 27 populations of European whitefish (Coregonus lavaretus) from nine lakes distributed in three neighboring subarctic watercourses in northern Fennoscandia as a model to test the importance of random drift versus diversifying natural selection for parallel evolution of adaptive phenotypic traits. We contrasted variation for two key adaptive phenotypic traits correlated with resource utilization of polymorphic fish; the number of gill rakers and the total length of fish, with the posterior distribution of neutral genetic differentiation from 13 microsatellite loci, to test whether the observed phenotypic divergence could be achieved by random genetic drift alone. Our results show that both traits have been under diversifying selection and that the evolution of these morphs has been driven by isolation through habitat adaptations. We conclude that diversifying selection acting on gill raker number and body size has played a significant role in the ongoing adaptive radiation of European whitefish morphs in this region.     

Differences in gill raker morphology between two local populations of a benthophagous filter-feeding fish, Goniistius zonatus (Cheilodactylidae)

Gill raker morphology of a benthophagous fish Goniistius zonatus (Cheilodactylidae) (10.9–29.2 cm SL), using a filter-feeding mode, was compared between two locations (Morode and Arakashi) in southern Japan. Although gill raker number and gill raker length at the two locations did not differ, gill raker spacing was narrower relative to overall fish size at Morode than at Arakashi, mainly because gill raker width was greater at Morode. The difference of gill raker spacing is unlikely to have a genetic or physiochemical explanation. Small invertebrates (≤1.0 mm) were dominant on the substrate at Morode but were less common at Arakashi. Such small animals were consumed by many fish at Morode but were rarely exploited at Arakashi. At Morode, the narrow gill raker spacing would be effective in retaining small prey, which should be an important energy resource in this population. The difference of interraker spacing at the two locations seems to be related to available prey size at each location. Received: November 14, 2000 / Revised: February 13, 2001 / Accepted: February 28, 2001     

Feeding habits and gill raker morphology of three planktivorous pelagic fish species off the coast of northern and western Kyushu in summer

Feeding habits and gill raker morphology were examined for the three major planktivorous pelagic fishes, Japanese anchovy Engraulis japonicus , Pacific round herring Etrumeus teres and Japanese jack mackerel Trachurus japonicus , off the northern and western coasts of Kyushu, in the north‐eastern part of the East China Sea in the summer months of 2001. Using fishes in the same size range (80–140 mm, standard length), the stomach contents of the three fish species were compared. The diet of the Japanese anchovy mainly consisted of Oncaeidae copepods, while the diets of the Pacific round herring and Japanese jack mackerel were dominated by calanoid copepods at all stations. Comparisons between prey size in the stomach, zooplankton size in the water and gill raker morphology suggested that the stomach contents of the three species were characterized mainly by the difference in the feeding behaviour between Japanese anchovy (filter‐feeding) and the other two species (particulate‐feeding), rather than by the difference in the morphology of feeding apparatus only. It was concluded that behavioural adaptations in the feeding of these pelagic fishes brought about trophic partitioning to some degree in this pelagic ecosystem in summer. Although the diets of these three species overlapped to some extent, there was still little likelihood of competition between the Japanese anchovy and the other two species. The potential for competition between the Pacific round herring and the Japanese jack mackerel is discussed.     

Trophic ecology and gill raker morphology of seven catostomid species in Iowa rivers

Understanding the trophic ecology of closely‐related species is important for providing insight on inter‐specific competition and resource partitioning. Although catostomids often dominate fish assemblages in lotic systems, little research has been conducted on their ecology. This study was developed to provide information on the trophic ecology of catostomids in several Iowa rivers. Food habits, diet overlap, and gill raker morphology were examined for highfin carpsucker Carpiodes velifer, quillback C. cyprinus, river carpsucker C. carpio, golden redhorse Moxostoma erythrurum, shorthead redhorse M. macrolepidotum, silver redhorse M. anisurum, and northern hogsucker Hypentelium nigricans sampled from four Iowa rivers (2009). Diet overlap among all species was calculated with Morista’s index (C). Food habit niche width was quantified with Levin’s index (B) and similarity in gill raker morphology was compared with analysis of covariance. Values from Morista’s index suggested significant overlap in the diets of highfin carpsucker and river carpsucker (C = 0.81), quillback and river carpsucker (C = 0.66), and shorthead redhorse and silver redhorse (C = 0.67). Levin’s index indicated that golden redhorse (B = 0.32), quillback (B = 0.53), and river carpsucker (B = 0.41) had the most generalized feeding strategies as their food niche widths were substantially wider than the other species. Gill raker length and spacing were positively correlated with the standard length of the fish for all species (gill raker length: r² = 0.67–0.88, P ≤ 0.01; gill raker spacing: r² = 0.63–0.73, P ≤ 0.01). Slopes of regression of gill raker length and spacing to standard lengths were significantly (P ≤ 0.05) different among species, indicating that rates of change in gill raker morphology with body length varied among species. Differences in gill raker morphology likely allow catostomids to partition resources and reduce competitive interactions.     

Sieving functional morphology of the gill raker feeding apparatus of atlantic menhaden

Menhaden occupy an important position in estuarine food webs, thus the rate processes associated with their feeding are critical to the ecosystem management of fishery and ecological resources. Atlantic menhaden feed on a wide range of plankton, the size and food quality of which change ontogenetically. We analyzed the functional morphology of the menhaden feeding apparatus in a size series of menhaden representative of juveniles and the adult migratory stock. The physical dimensions of gill arches and rakers increased isometrically with fish length; however, branchiospinule spacing, the dimension that forms the sieve apertures of the branchial basket, scaled allometrically with fish length. Juvenile menhaden from North Carolina have branchiospinule spacings that averaged 12 microm, with three arch subsections of average spacing < 10 microm. Spacings did not increase with juvenile growth until the first allometric inflection point at approximately 100 mm fork length (FL). Spacing data for juveniles from other locations suggests spacing increases with latitude. Spacings increase with fish length in adults until a second inflection at 200 mm FL, after which spacing averages 37 microm. These data suggest menhaden juveniles filter smaller plankton with higher filtration efficiency than previously considered and that regional recruitment may affect adult distribution through foraging preferences.     

鱼体(去鳃)和鱼鳃对不同形态铜的积累特征

在实验室条件下研究实验鱼Ｐａｒａｃｈｅｉｒｏｄｏｎ对人工河水中不同形态的积累特征,对比了鱼体（去鳃）和鱼鳃对铜吸收量的差异,并探讨了鱼对铜的吸收机理。研究结果表明,实验鱼鳃部和体内铜积累量均随水相游离铜浓度增高,暴露时间增长而增加,但鳃部积累浓度较鱼体其余部分高一个数量级,其从水相富集铜的速率显著高于鱼体。     

The role of environmental sodium chloride relative to calcium in gill morphology of freshwater salmonid fish

Summary Ultrastructure, distribution and abundance of cell types were examined in the gills of two freshwater salmonid species, Salmo fario and Salmo gairdneri, in media of selected ion content. In plain hard water (PW) with high concentrations of Ca²⁺, Na⁺, and Cl^-, gill chloride cells (CC) were confined to trailing edges and interlamellar regions of filaments whereas in mountain soft water (MW) with low concentrations of Ca²⁺, Na⁺, and Cl^-, CC were more numerous on filaments and covered lamellae, particularly along trailing edges. CC also appeared on lamellae of PW trout acclimated to soft water in a pond. This proliferation was not alleviated when ambient Ca²⁺ levels were raised (MW + Ca²⁺) but regressed in elevated NaCl media (MW + NaCl). The regression process involved an initial covering of CC by pavement cells followed by cytolysis and then eventual disappearance of CC. In MW, mucous cells were distributed mainly on trailing edges and, to a lesser extent, leading edges of filaments; they were absent from lamellae regardless of external ion levels.The results of this study shed some light on the functional significance of CC in freshwater fish. It is suggested that proliferation of CC is an adaptive response to dilute freshwater (i.e. [NaCl]<0.1 mequiv·1^-1).     

Generation of a neutral FST baseline for testing local adaptation on gill raker number within and between European whitefish ecotypes in the Baltic Sea basin

Divergent selection at ecologically important traits is thought to be a major factor driving phenotypic differentiation between populations. To elucidate the role of different evolutionary processes shaping the variation in gill raker number of European whitefish (Coregonus lavaretus sensu lato) in the Baltic Sea basin, we assessed the relationships between genetic and phenotypic variation among and within three whitefish ecotypes (sea spawners, river spawners and lake spawners). To generate expected neutral distribution of F_ST and to evaluate whether highly variable microsatellite loci resulted in deflated F_ST estimates compared to less variable markers, we performed population genetic simulations under finite island and hierarchical island models. The genetic divergence observed among (F_CT = 0.010) and within (F_ST = 0.014–0.041) ecotypes was rather low. The divergence in gill raker number, however, was substantially higher between sea and river spawners compared to observed microsatellite data and simulated neutral baseline (P_CT > F_CT). This suggests that the differences in gill raker number between sea and river spawners are likely driven by divergent natural selection. We also found strong support for divergent selection on gill raker number among different populations of sea spawners (P_ST > F_ST), most likely caused by highly variable habitat use and diverse diet. The putative role of divergent selection within lake spawners initially inferred from empirical microsatellite data was not supported by simulated F_ST distributions. This work provides a first formal test of divergent selection on gill raker number in Baltic whitefish, and demonstrates the usefulness of population genetic simulations to generate informative neutral baselines for P_ST–F_ST analyses helping to disentangle the effects of stochastic evolutionary processes from natural selection.     

African cichlid fish: a model system in adaptive radiation research

The African cichlid fish radiations are the most diverse extant animal radiations and provide a unique system to test predictions of speciation and adaptive radiation theory. The past few years have seen major advances in the phylogenetics, evolutionary biogeography and ecology of cichlid fish. Most of this work has concentrated on the most diverse radiations. Unfortunately, a large number of small radiations and 'non-radiations' have been overlooked, potentially limiting the contribution of the cichlid system to our understanding of speciation and adaptive radiation. I have reviewed the literature to identify 33 intralacustrine radiations and 76 failed radiations. For as many as possible I collected information on lake size, age and phylogenetic relationships. I use these data to address two questions: (i) whether the rate of speciation and the resulting species richness are related to temporal and spatial variation in ecological opportunity and (ii) whether the likelihood of undergoing adaptive radiation is similar for different African cichlid lineages. The former is a key prediction of the ecological theory of adaptive radiation that has been presumed true but remains untested for cichlid radiations. The second is based on the hypothesis that the propensity of cichlids to radiate is due to a key evolutionary innovation shared by all African cichlids. The evidence suggests that speciation rate declines through time as niches get filled up during adaptive radiation: young radiations and early stages of old radiations are characterized by high rates of speciation, whereas at least 0.5 Myr into a radiation speciation becomes a lot less frequent. The number of species in cichlid radiations increases with lake size, supporting the prediction that species diversity increases with habitat heterogeneity, but also with opportunity for isolation by distance. Finally, the data suggest that the propensity to radiate within lakes is a derived property that evolved during the evolutionary history of some African cichlids, and the appearance of which does not coincide with the appearance of proposed key innovations in morphology and life history.     

Vascular anatomy of the fish gill

The fish gill is the most physiologically diversified vertebrate organ, and its vasculature the most intricate. Application of vascular corrosion techniques that couple high-fidelity resins, such as methyl methacrylate, with scanning electron microscopy yields three-dimensional replicas of the microcirculation that have fostered a better appreciate gill perfusion pathways. This is the focus of the present review. Three vascular networks can be identified within the gill filament. The arterioarterial (respiratory) pathway consists of the lamellae and afferent and efferent segments of the branchial and filamental arteries and lamellar arterioles. The body of the filament contains two post-lamellar pathways: the interlamellar and nutrient. The interlamellar system is an extensive ladder-like network of thin-walled, highly distensible vessels that traverses the filament between, and parallel to, the lamellae and continues around the afferent and efferent borders of the filament. Interlamellar vessels are supplied by short, narrow-bore feeder vessels from the medial wall of the efferent filamental artery. A myriad of narrow-bore, tortuous arterioles arise from the basal efferent filamental artery and efferent branchial artery and anastomose to form the nutrient circulation of the arch and filament. In the filament body, nutrient capillaries and interlamellar vessels are often closely associated, and the former may ultimately drain into the latter. Many of the anatomical characteristics of interlamellar vessels are strikingly similar to those of mammalian lymphatic capillaries, with the exception that interlamellar vessels are directly fed by arteriovenous-like anastomoses. It is likely that gill interlamellar and mammalian lymphatics are physiologically, if not embryologically, equivalent.     

Site preference of fish myxosporeans in the gill

In addition to the morphological and size characteristics of the spores, indicating the exact location and tissue specificity is also essential for differentiation of the large number of species belonging to the group of gill-parasitic fish, the myxosporeans. According to the observations of the present author, Myxobolus, Henneguya and Thelohanellus species are characterised by strict tissue specificity, and species showing affinity to the epithelium, connective tissue, cartilage or vascular tissue usually occur in a strictly defined location within the gill apparatus. Some of the species typically form plasmodia in the lamellae of the gill and others in the gill filaments. Yet other species develop their plasmodia at the base of the gill filament or in the gill arch. Instead of the generally accepted but misleading terms 'intra-' and 'interlamellar', the present author distinguishes interlamellar-epithelial and intralamellar-vascular types in the case of plasmodia developing in the gill lamellae, and intrafilamental-epithelial, intrafilamental-vascular and intrafilamental-chondroidal types in the case of plasmodia developing in the gill filaments. Regarding site of development within the gill, the location of basifilamental plasmodia and that of plasmodia developing in the cartilaginous matrix, connective tissue or blood vessels of the gill arch are well distinguishable from the above types. The different types and their variations are shown in histological illustrations.     

Salinity adaptation in fish: interaction of thyroxine with fish gill mitochondria

When the freshwater fish Sarotherodon mossambicus is exposed to an ionoosmotic stress, extensive changes take place in the energetics of the gill mitochondria. These changes are reversed when thyroxine is administered to the fish prior to exposure to stress [K. Shivakumar and J. Jayaraman (1984) Arch. Biochem. Biophys. 233, 728]. The presence of a thyroxine binding component in the mitochondrial inner membrane, its characteristics, and its possible involvement in the salinity adaptation process are discussed.     

Identification of palearctic coregonid fish species using mtDNA and allozyme genetic markers

Two types of molecular genetic markers were used for genetic identification of species and local stocks of palearctic coregonids (Coregonidae, Salmoniformes, Teleostei). Seven nominate species of whitefishes and ciscoes Coregonus , spp. of Eurasia Arctic Sea basin and inconnu Stenodus leucichthys nelma , represented by specimens from North America were studied. Using restriction analysis of PCR-amplified products of the ND-1 gene of mitochondrial DNA (mtDNA) and allelic composition at several allozyme loci discrimination was successful between C. lavaretus pidschian , Siberian whitefish, C. nasus , broad whitefish, C. autumnalis , Arctic cisco, C. migratorius , Baikal omul, C. peled , peled, and C. sardinella , least cisco. Muksun C. muksun , was indistinguishable from Siberian whitefish. Creatine kinase (CK) isozyme patterns and Rsa , I restriction patterns of ND-1 were the most effective markers allowing discrimination among species. Intra-specific differentiation in mtDNA was found in all species but was much less pronounced than inter-species variation. In several specimens composite haplotypes typical of another species were found that reflect probable gene introgression by hybridization. A combination of mtDNA and nuclear genetic markers is suggested for reliable identification of both typical species representatives and hybrids.     

Non-infectious gill disorders of marine salmonid fish

Gill disorders present a significant challenge in salmon (Salmo salar and Oncorhynchus sp.) farming regions throughout the world. This review of gill disorders and diseases of marine fish is focused on the non-infectious causes of gill disease in marine stage salmonids and these are grouped into harmful algae, such as Karenia mikimotoi, harmful zooplankton, such as Pelagia noctiluca, other environmental challenges, such as pollutants, as well as nutritional and genetic or congenital causes. The present level of understanding of these gill disorders is reviewed with regard to risk factors, potential impacting factors, methods of best practice to mitigate non-infectious gill disease and disorders, as well as knowledge gaps and avenues for future research.     

Heritability and adaptive significance of the number of egg-dummies in the cichlid fish Astatotilapia burtoni

Cichlid fishes are a textbook example of rapid speciation and exuberant diversity--this applies especially to haplochromines, a lineage with approximately 1800 species. Haplochromine males uniquely possess oval, bright spots on their anal fin, called 'egg-spots' or 'egg-dummies'. These are presumed to be an evolutionary key innovation that contributed to the tribe's evolutionary success. Egg-spots have been proposed to mimic the ova of the mouthbrooding females of the corresponding species, contribute to fertilization success and even facilitate species recognition. Interestingly, egg-spot number varies extensively not only between species, but also within some populations. This high degree of intraspecific variation may appear to be counterintuitive since selection might be expected to act to stabilize traits that are correlated with fitness measures. We addressed this 'paradox' experimentally, and found that in the haplochromine cichlid Astatotilapia burtoni, the number of egg-spots was related to male age, body condition and dominance status. Intriguingly, the egg-spot number also had a high heritable component (narrow sense heritability of 0.5). These results suggest that the function of egg-spots might have less to do with fertilization success or species recognition, but rather relate to mate choice and/or male-male competition, helping to explain the high variability in this important trait.     

Population genomic tests of models of adaptive radiation in Lake Victoria region cichlid fish

Adaptive radiation is usually thought to be associated with speciation, but the evolution of intraspecific polymorphisms without speciation is also possible. The radiation of cichlid fish in Lake Victoria (LV) is perhaps the most impressive example of a recent rapid adaptive radiation, with 600+ very young species. Key questions about its origin remain poorly characterized, such as the importance of speciation versus polymorphism, whether species persist on evolutionary time scales, and if speciation happens more commonly in small isolated or in large connected populations. We used 320 individuals from 105 putative species from Lakes Victoria, Edward, Kivu, Albert, Nabugabo and Saka, in a radiation-wide amplified fragment length polymorphism (AFLP) genome scan to address some of these questions. We demonstrate pervasive signatures of speciation supporting the classical model of adaptive radiation associated with speciation. A positive relationship between the age of lakes and the average genomic differentiation of their species, and a significant fraction of molecular variance explained by above-species level taxonomy suggest the persistence of species on evolutionary time scales, with radiation through sequential speciation rather than a single starburst. Finally the large gene diversity retained from colonization to individual species in every radiation suggests large effective population sizes and makes speciation in small geographical isolates unlikely.