North American Cyprinid Fishes Research Articles

High background risk induces risk allocation rather than generalized neophobia in the fathead minnow

AbstractTo cope with the heterogeneous nature of predation and the trade-off between predator avoidance and foraging, prey animals have evolved several cognitive rules. One of these is the risk allocation hypothesis, which predicts that in environments with long periods of sustained high risk, individuals should decrease their antipredator effort to satisfy their metabolic requirements. The neophobia hypothesis, in turn, predicts increased avoidance of novel cues in high-risk habitats. Despite the recent interest in predator-induced neophobia across different sensory channels, tests of such generalized neophobia are restricted to a single fish taxon, the Cichlidae. Hence, we retested the generalized neophobia hypothesis in fathead minnows Pimephales promelas, a small schooling North American cyprinid fish. From hatching onward, minnows were exposed to conspecific alarm cues, which indicate predation risk, or distilled water in a split-clutch design. After 1 month, shoaling behavior was examined prior and subsequent to a mechanical predator disturbance. Fish previously exposed to elevated background risk formed compact shoals for a shorter time interval after the stimulus compared with controls. These results contrast previous studies of generalized neophobia but match the risk allocation hypothesis. Consequently, risk allocation and generalized neophobia are not ubiquitous cognitive rules but instead evolved adaptations of different taxa to their respective environments.

Morphological and genetic evolution in eastern populations of the Macrhybopsis aestivalis complex (Cypriniformes: Cyprinidae), with the descriptions of four new species.

For many years the North American cyprinid fish Macrhybopsis aestivalis (common name: Speckled Chub) was regarded as a single widespread and morphologically variable species, occurring in rivers throughout much of the Mississippi Valley and geographically adjacent eastern Gulf slope drainages, west to the Rio Grande basin in Texas, New Mexico, and Mexico. Eisenhour (1997) completed a morphological study of western populations of the Speckled Chub, the results of which appeared thereafter in published form (Eisenhour 1999, 2004). He demonstrated the existence of five valid species west of the Mississippi River (aestivalis, marconis, australis, tetranema, hyostoma), of which the name aestivalis was shown to be restricted to the population occurring in the Rio Grande and the geographically adjacent Rio San Fernando system, in northeastern Mexico. Eisenhour (2004) considered populations throughout the middle Mississippi Valley and its major tributaries to be a single morphologically variable species (hyostoma), and he also indicated that populations of Macrhybopsis from eastern Gulf slope drainages may represent a complex of species. Genetic confirmation of Eisenhour's conclusions regarding western species appeared in the publication by Underwood et al. (2003), who also showed that western populations of M. hyostoma, as presently recognized, are genetically much more complex than previously considered. Meanwhile, the present authors were involved in a companion study of eastern populations of Macrhybopsis, for which a genetic summary of the eastern Gulf coast species was published by Mayden & Powers (2004). Based on their findings, four species were recognized from southeastern drainages (identified as species A-D), although no formal taxonomic descriptions were included. Their genetic data, in combination with meristic, morphometric and other morphological data presented herein, form the basis for a revised classification of eastern Macrhybopsis populations, including formal descriptions of the four new species from eastern Gulf coast drainages.

Phylogeny and genetic variation within the widely distributed Bluntnose Minnow, Pimephales notatus (Cyprinidae), in North America.

This study represents a phylogenetic analysis of Pimephales notatus, a widely distributed North American cyprinid fish species, using one mitochondrial (cytb) and two nuclear (S7 and Rag1) genes. Despite the broad geographic distribution of this species that includes independent basins, results suggest a largely drainage-independent genetic structure. Results reveal a well-supported lineage in the Ozark Highlands, which is highly divergent from the remaining populations and may represent a long-term isolated lineage that should be considered as a separate conservation and management unit. All other remaining populations comprised a widely distributed lineage, covering most of the distribution for the species (from the Red River and tributaries of the Great Lakes in the north to the lower Mississippi and Mobile basin in the south, and from the Missouri River in the west to the Chesapeake and Albemarle Sound basins in the east). Phylogenetic, genetic diversity, and biogeographical data suggest that this wide-ranging lineage could have experienced a recent expansion to northern areas where populations exhibit little genetic variation. Results from molecular analyses reveal a distinctive lineage in the Ozarks and suggest that there is need for morphological analyses within P. notatus to determine its taxonomic status.

Reconciling gene trees of eastern North American minnows

Most eastern North American cyprinid fishes belong to a clade known as the “open posterior myodome” (OPM) minnows, but phylogenetic relationships within this clade have been difficult to ascertain. Previous attempts to resolve relationships among the generally benthic “chubs” and the more pelagic “shiners”, that constitute the majority of OPM minnows, have led to highly discordant phylogenetic hypotheses. To further examine relationships among the OPM minnows, we utilized both a concatenated Bayesian approach and a coalescent-based species tree method to analyze data from six protein coding nuclear loci (Enc1, Ptr, Ryr3, Sh3px3, Tbr1, and Zic1), as well as the mitochondrial locus (Cytb). We focused our analyses on the chub-like genus Phenacobius, a group that has drifted topologically between other benthic chubs and the more pelagic shiners, and also included exemplar taxa from 11 other OPM lineages. Individual gene trees were highly discordant regarding relationships within Phenacobius and across the OPM clade. The concatenated Bayesian analysis and coalescent-based species tree reconstruction recovered slightly different phylogenetic topologies. Additionally, the posterior support values for clades using the coalescent-based approach were consistently lower than the concatenated analysis. However, Phenacobius was resolved as monophyletic and as the sister lineage to Erimystax regardless of the combined data approach taken. Furthermore, Phenacobius+Erimystax was recovered as more closely related to the shiners we examined than to other chubs. Relationships within Phenacobius varied depending on the combined phylogenetic method utilized. Our results highlight the importance of multi-locus, coalescent-based approaches for resolving the phylogeny of diverse clades like the eastern North American OPM minnows.

Isolation and characterization of major histocompatibility class IIβ genes in an endangered North American cyprinid fish, the Rio Grande silvery minnow ( Hybognathus amarus)

The major histocompatibility complex (MHC) is a critical component of the adaptive immune response in vertebrates. Due to the role that MHC plays in immunity, absence of variation within these genes may cause species to be vulnerable to emerging diseases. The freshwater fish family Cyprinidae comprises the most diverse and species-rich group of freshwater fish in the world, but some are imperiled. Despite considerable species richness and the long evolutionary history of the family, there are very few reports of MHC sequences (apart from a few model species), and no sequences are reported from endemic North American cyprinids (subfamily Leuciscinae). Here we isolate and characterize the MH Class II beta genes from complementary DNA and genomic DNA of the non-model, endangered Rio Grande silvery minnow ( Hybognathus amarus), a North American cyprinid. Phylogenetic reconstruction revealed two groups of divergent MH alleles that are paralogous to previously described loci found in deeply divergent cyprinid taxa including common carp, zebrafish, African large barb and bream. Both groups of alleles were under the influence of diversifying selection yet not all individuals had alleles belonging to both allelic groups. We concluded that the general organization and pattern of variation of MH class II genes in Rio Grande silvery minnow is similar to that identified in other cyprinid fishes studied to date, despite distant evolutionary relationships and evidence of a severe genetic bottleneck.

Do constructional constraints influence cyprinid (Cyprinidae: Leuciscinae) craniofacial coevolution?

Constraints on form may determine how organisms diversify. As a result of competition for the limited space within the body, investment in adjacent structures could represent an evolutionary compromise. For example, evolutionary trade-offs resulting from limited space in the head could have influenced how the sizes of the jaw muscle, as well as the eyes, evolved in North American cyprinid fishes. To test the evolutionary independence of the size of these structures, we measured the mass of the three major adductor mandibulae muscles and determined the eye volume in 36 cyprinid species. Using a novel phylogeny, we tested the hypotheses that the sizes of these four structures were negatively correlated with each other during cyprinid evolution. We found that evolutionary change in the adductor mandibulae muscles was generally positively and/or not correlated, suggesting that competition for space among cyprinid jaw muscles has not influenced their evolution. However, there was a negative relationship between mass of adductor mandibulae 1 and eye volume, indicating that change in these physically adjacent structures is consistent with an evolutionary constructional constraint. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103, 136–146.

Cytogenetic studies in North American minnows (Cyprinidae): Chromosomal NOR phenotypes of 12 species, with comments on cytosystematic relationships among 50 species

Chromosomal NOR phenotypes are documented for twelve species of North American cyprinid fishes whose NOR karyotypes have not been previously reported. Patterns of interspecific chromosomal NOR variation are then summarized for the fifty species of North American cyprinids surveyed to date. The degree of interspecific NOR variation among North American cyprinids suggests that the rate of chromosomal evolution within the group may have been higher than previously believed. The interspecific variants in chromosomal NORs are used as taxonomic and systematic characters in order to infer phylogenetic hypotheses of species relationships. The phylogenetic inferences drawn from the chromosomal NOR data provide a framework upon which future cytosystematic studies in North American cyprinids can be based.

Phylogenetic relationships of the enigmatic ornate shiner, Cyprinella ornata, a species endemic to Mexico (Teleostei: Cyprinidae)

The systematics and taxonomy of North Americancyprinid fishes has historically been said tobe in a chaotic state of affairs. Much of theconfusion as to relationships of species restsin the lack of explicit phylogenetic hypothesesof species and reliance upon degree ofdistinctiveness of taxa or their overallsimilarity for generic placement. Some specieshave had more turbulent or variable taxonomichistories than others. The ornate shiner, Cyprinella ornata, is one of those species,having been placed in the genera Notropis,Codoma, and Cyprinella within the last20 years and found in current texts in any ofthese three genera. Most of the confusionregarding placement of this species has beenrelated to lack of explicit phylogenetichypotheses to formulate its classification, butto a certain degree some researchers haveignored phylogenetic studies and preferred torely upon its morphological distinctiveness orreproductive behavioral traits of questionablehomology to place it in a monotypic genus andalign it with the genera Pimephales andOpsopoeodus.I present a phylogenetic analysis based oncomplete Cytochrome b sequences fromornate shiners, other species of Cyprinella, purported relatives, and severalother species of the Shiner Clade to determinethe phylogenetic affinities of this enigmaticspecies. Molecular analysis reveals the ornateshiner to be more closely related to species ofCyprinella than to a Pimephalesplus Opsopoeodus clade as previouslydiscussed in one morphological analysis, or asargued by Page and Johnston (1990), Johnstonand Page (1992) and Page and Ceas (1989) basedon observations of spawning behaviors andhypotheses of homology between crevice-spawningand egg-clumping behaviors. This molecularanalysis is more consistent with earliermorphological phylogenetic hypotheses of Mayden(1989) wherein these two clades are notconsidered to be closely related and the ornateshiner is a member of the genus Cyprinella.

Phylogenetic Relationships of the Creek Chubs and the Spine-Fins: an Enigmatic Group of North American Cyprinid Fishes (Actinopterygii: Cyprinidae).

Phylogenetic analyses based on the complete nucleotide sequence of the mitochondrial 12S ribosomal RNA gene were performed for representatives of major North American cyprinid clades. These analyses resolved four monophyletic groups: (1) Western Clade, represented by Acrocheilus and Gila, (2) Creek Chub Clade, represented by Couesius, Hemitremia, Semotilus, and Margariscus, (3) Open Posterior Myodome Clade, represented by Campostoma, Phenacobius, Cyprinella, Notropis, Platygobio, and Rhinichthys, and (4) Plagopterin Clade, represented by Snyderichthys, Lepidomeda, and Meda. The overall results of these analyses refute previous hypotheses of relationships of North American Cyprinidae based on morphological data. Our analyses support recognition of Snyderichthys, formerly considered a subgenus of Gila, and indicate that the Plagopterin Clade is sister to the Creek Chub Clade. Furthermore, this analysis indicates that hypotheses of relationship between plagopterins and other Western taxa are unsupported and the Open Posterior Myodome Clade is a monophyletic group.

Phylogenetic Relationships of the Creek Chubs and the Spine-Fins: an Enigmatic Group of North American Cyprinid Fishes (Actinopterygii: Cyprinidae)

Phylogenetic analyses based on the complete nucleotide sequence of the mitochondrial 12S ribosomal RNA gene were performed for representatives of major North American cyprinid clades. These analyses resolved four monophyletic groups: (1) Western Clade, represented byAcrocheilusandGila, (2) Creek Chub Clade, represented byCouesius,Hemitremia,Semotilus, andMargariscus, (3) Open Posterior Myodome Clade, represented byCampostoma,Phenacobius,Cyprinella,Notropis,Platygobio, andRhinichthys, and (4) Plagopterin Clade, represented bySnyderichthys,Lepidomeda, andMeda. The overall results of these analyses refute previous hypotheses of relationships of North American Cyprinidae based on morphological data. Our analyses support recognition ofSnyderichthys, formerly considered a subgenus ofGila,and indicate that the Plagopterin Clade is sister to the Creek Chub Clade. Furthermore, this analysis indicates that hypotheses of relationship between plagopterins and other Western taxa are unsupported and the Open Posterior Myodome Clade is a monophyletic group.

Evolution of the Cyprinella lutrensis species group. III. Geographic variation in the mitochondrial DNA of Cyprinella lutrensis — the influence of Pleistocene glaciation on population dispersal and divergence

We employed restriction site variation in mitochondrial (mt)DNA to determine if significant phylogeographic structure occurs in the North American cyprinid fish Cyprinella lutrensis. Digestion patterns from 16 restriction endonucleases identified fifty mtDNA haplotypes among 127 individuals of Cyprinella lutrensis assayed from localities in the Gulf Coastal Plain, the Great Plains, and the Central Lowlands. Nucleotide sequence divergence among haplotypes was highly variable (mean ± SE: 2.87%± 0.08; range: 0.14–9.24%). Maximum-parsimony analysis and the neighbour joining method of tree construction revealed three major groupings (clades) of haplotypes that differed in geographic distribution. Divergence estimates between the basal clade, comprised of haplotypes primarily from the Brazos River in east Texas, and the remaining two clades, place C. lutrensis in the western Gulf Coastal Plain prior to Pleistocene glaciation. Nucleotide sequence divergence between the second clade, comprised of haplotypes from the Trinity and Calcasieu rivers in east Texas and southwestern Louisiana, respectively, and the third clade (comprised primarily of haplotypes from localities north of Texas and affected directly by Pleistocene glaciation), suggest that C. lutrensis colonized gladated regions to the north during the mid- to late Pleistocene. This hypothesis is supported by levels of intrapopulational nucleotide diversity in geographic localities outside of Texas and by geological evidence. Despite marked geographic variation in morphometries, meristics, and nuptial coloration, mtDNA variation in glaciated regions was not geographically structured, and subspecies of C. lutrensis were not identifiable by phylogenetic analysis of mtDNA.

A Molecular Perspective on the Phylogenetic Relationships of the Barbeled Minnows, Historically Assigned to the Genus Hybopsis (Cyprinidae: Cypriniformes)

Allozyme products of 32 gene loci were compared for the North American cyprinid fishes Campostoma oligolepis, Cyprinella galactura, Cyprinella monacha, Erimystax cahni, E. dissimilis, E. insignis, E. x-punctatus, Hybopsis amblops, H. labrosa, H. rubriforns, H. zanema, Macrhybopsis aestivalis, M. gelida, M. meeki, Nocomis biguttatus, Phenacobius uranops, Platygobio gracilis, and P. storeriana. Triose-phosphate isomerase was found to be duplicated in all species examined. Parsimony analysis revealed that Hybopsis sensu lato did not form a monophyletic group. Cyprinella monacha was found to be the sister species to members of the genus Cyprinella and was excluded from the genus Erimystax. A clade of four species of Erimystax was identified although relationships among the four species could not be resolved. Phenacobius was identified as the sister group to Erimystax. The genus Macrhybopsis was expanded to include M. aestivalis. Macrhybopsis gelida was identified as the sister to M. meeki and M. aestivalis as the sister to the former two species. The genus Platygobio was expanded to include P.storeriana. Hybopsis labrosa and H. zanema were found to be more closely related to members of the genus Hybopsis sensu stricto than to members of Cyprinella.

Cytogenetic studies in North American minnows (Cyprinidae). XXII. Chromosomal nucleolar organizer regions in the genus Pimephales

Chromosomal nucleolar organizer region (NOR) phenotypes are documented for all four extant species in the North American cyprinid fish genus Pimephales. All four species (P. notatus, P. promelas, P. tenellus, and P. vigilax) possess 2n = 50 chromosomes and a pair of NOR-bearing chromosomes with the NOR situated terminally on the short arm of a medium-sized to large submetacentric chromosome (NOR phenotype C). Trypsin G-banding demonstrated that the C NOR chromosome in all four species is homologous. Two of the species (P. tenellus and P. promelas) also possess a C′ NOR chromosome, which is defined as an NOR situated terminally on the short arm of a large submetacentric chromosome that is also the largest chromosome in the complement. The C′ NOR chromosome occurs infrequently in P. promelas, being found in only 8% or so of all metaphases examined. Trypsin G-banding demonstrated that the C′ NOR chromosomes in the two Pimephales species are homologous to one another and to the C′ NOR chromosomes found in the cyprinid genus Cyprinella. A presumed derivative of the C′ NOR chromosome occurs in the monotypic cyprinid genus Opsopoeodus. The NOR chromosomal data support monophyly of the four extant species of Pimephales, and further suggest that the genus Pimephales belongs in a monophyletic assemblage with, among others, the cyprinid genera Cyprinella and Opsopoeodus. The data do not support the previous hypothesis that Pimephales is a basal clade outside of a larger assemblage of "Notropis"-like, shiners.

Intraspecific Variation in Chromosomal Nucleolus Organizer Regions in Notropis chrysocephalus (Pisces: Cyprinidae)

ganizer regions (NORs) in North American cyprinid fishes and using the data to infer hypotheses of species or species-groups relationships (Gold and Amemiya, 1986; Amemiya and Gold, 1988; Gold et al., 1988). Thus far, we have surveyed chromosomal NOR phenotypes of nearly 50 cyprinid species (Amemiya and Gold, 1988; Gold et al., 1988; J. R. Gold, pers. obser.), the majority of which belong to the extremely speciose genus Notropis. The NORs themselves are the chromosomal sites for the 18S and 28S ribosomal

Genome size variation and evolution in North American cyprinid fishes

Genome size variation and evolution in North American cyprinid fishes

Genome size variation and evolution in North American cyprinid fishes

Genome size variation and evolution in North American cyprinid fishes

Cytogenetic studies in North American minnows(Cyprinidae). XVIII. Chromosomal NOR variation among eight species.

The karyotypes and chromosomal nucleolus organizer region or NOR phenotypes of eight species of North American cyprinid fishes are documented. All eight species possessed 2n=50 chromosomes. Four species (Cyprinella formosa, Cyprinella gibbsi, Notropis boops, and Notropis dorsalis) possessed only a single pair of NOR-bearing chromosomes, whereas four species (Notropis petersoni, Notropis sabinae, Phenacobius mirabilis, and Semotilus atromaculatus) possessed multiple NORs, i. e., more than one pair. The phylogenetic implications of the chromosomal NOR data in the eight species are discussed relative to current concepts of North American cyprinid systematics based largely on morphological data. A phylogenetic hypothesis based on chromosomal NOR and other data is presented for 11 species of the cyprinid genus Cyprinella, and our previous hypothesis that a single pair of NOR chromosomes is the plesiomorphic NOR state for a large eastern North American cyprinid lineage is questioned.

Genome size variation in the North American sunfish genusLepomis(Pisces: Centrarchidae)

SummaryGenome sizes (nuclear DNA contents) were documented spectrophotometrically from individuals of each of nine species of the North American centrarchid (sunfish) genusLepomis. The distributions of DNA values within and among the nine species were essentially normal and continuous, suggesting that changes in DNA quantity inLepomisare small in amount, involve both gains and losses of DNA, and are cumulative and independent in effect. Significant differences in mean genome size were found between individuals within populations in all nine species and between species. Nested analysis of variance and comparisons of average genome size difference or distance between individuals drawn from different levels of taxonomic organization revealed that the majority of genome size divergence inLepomisoccurs above the hierarchical level of individuals within populations. TheLepomisdata when compared to similar data from North American cyprinid fishes appear to suggest that: (i) genome size evolution in these fishes at least follows a continuous rather than a discontinuous mode; (ii) the general predictions of hypothetical models relating genome size variation as a function of organismal position along adaptive continua may be oversimplified, or not applicable to complex, higher eukaryotes; and (iii) changes in genome size in these fishes may be concentrated in speciation episodes.

Origin of Brood Stock and Allozyme Variation in Hatchery-Reared Bonytail, an Endangered North American Cyprinid Fish

Brood stock of critically endangered bonytail Gila elegans was obtained between 1976 and 1981 from Lake Mohave, Arizona-Nevada, and propagated by artificial means and by natural reproduction in ponds at Dexter National Fish Hatchery, New Mexico. Twenty-four naturally produced F2 individuals were examined electrophoretically for soluble gene products of 45 loci. Six polymorphic loci were identified: aspartate aminotransferase (sAat-A), glucose-6-phosphate isomerase (Gpi-B), and phosphoglucomutase (Pgm-A) from skeletal muscle; esterase (Est-2) from brain; and catalase (Cat-1) and L-iditol dehydrogenase (Iddh-A) from liver. Electromorph distributions at each locus agreed with Hardy–Weinberg expectations. Hatchery bonytail had a lower mean level of heterozygosity than arroyo chub G. orcutti. However, direct-count heterozygosity for bonytail was comparable to mean values reported for other western North American cyprinids. Allozyme variation expressed by hatchery-produced bonytails suggested a genetically variable stock suitable for reintroductions into appropriate wild habitats.

Chromosomal NORs as taxonomic and systematic characters in North American cyprinid fishes

There is substantial interspecific variation in chromosomal NORs among North American cyprinid fishes. This variation is taxonomically informative. In addition, the chromosomal NOR database appears to provide a framework from which systematic or phylogenetic inferences can be made. Our present approach to making such inferences from chromosomal NOR data is discussed.