Results of Hybridization between Anadromous and Resident Forms of European River Lamprey <Emphasis Type="Italic">Lampetra fluviatilis</Emphasis>

Survival of the progeny obtained from artificial crossing of large parasitic anadromous and small nonparasitic resident European river lampreys Lampetra fluviatilis is analyzed. A high individual survival (~61% on average) up to the stage of prolarvae burrowing into ground confirms the absence of a postzygotic barrier between the lamprey forms. The obtained results are discussed in the framework of two theories: of paired species and of intraspecies diversity.     

Population structure of arctic lamprey <Emphasis Type="Italic">Lethenteron camtschaticum</Emphasis> from the Kol River (Western Kamchatka)

Phenetic diversity is investigated and the taxonomic status of lampreys (Petromyzontidae) from the Kol basin (Western Kamchatka) is verified. Typically anadromous lamprey, anadromous lamprey forma praecox, resident lamprey, smolts, and larvae of lamprey are discovered and described. Their comparative analysis is made by standard morphometric characters. Differences between the forms by plastic characters depend on size and weight. No significant differences are found by major taxonomic characters between the forms of anadromous and resident lampreys which would indicate their taxonomic separation. Phenetic types of spawners are representatives of the population of one complexly structured species represented by life forms realizing different life history strategies (anadromous and resident), and belong to the species Arctic lamprey Lethenteron camtschaticum (Tilesius, 1811).     

Oral Fimbriae and Papillae in Parasitic Lampreys (Petromyzontiformes)

There are 38 species of living lampreys, 18 parasitic and 20 nonparasitic. The parasitic species feed as adults, while the nonparasitic do not. The taxonomy and systematics of the living lampreys is based primarily on dentition characters. Since the number of oral fimbriae and oral papillae have never been systematically investigated in lampreys, we compared them in 17 of the 18 parasitic lampreys to assess their usefulness as taxonomic characters. Both showed little variation with total length and sex within a species, while exhibiting greater variation between species. Parasitic species belonging to the three lamprey families could be distinguished using the number of oral fimbriae: southern hemisphere Mordaciidae (0) and Geotriidae (55–65) and northern hemisphere Petromyzontidae (81–144). However, the taxonomic usefulness of the two characters at the species level was limited. Ten out of the 17 species of parasitic lampreys were placed into four distinct groups based on their numbers of oral fimbriae, and only in two of these was the character diagnostic. Twelve out of the 17 species were placed into two distinct groups based on their numbers of oral papillae and for none of these was the character diagnostic. Blood feeders and intermediate feeders (blood + flesh) were shown to have significantly higher numbers of oral fimbriae than flesh feeders. The higher numbers of oral fimbriae in the former two types of feeders were presumed to be linked to their greater need to create a good seal for feeding purposes. Blood feeders were also shown to have significantly higher numbers of oral papillae than either intermediates or flesh feeders. The higher numbers of oral papillae in the blood feeders were presumed to be linked to their greater need to find suitable attachment sites for feeding purposes.     

The urogenital papilla in the Holarctic lamprey (Petromyzontidae)

Synopsis The urogenital papillae of 30 species of Holarctic lampreys were examined to determine if this structure has any taxonornic use. Total length, branchial length and papilla length were measured. A correlation between mean papilla length and mean total length of the species existed in males for parasitic species but not nonparasitic species, indicating a potential use in nonparasitic species. In nonparasitic species the most obvious differences existed in the papilla length: branchial length ratio. From the limited material available there appeared to be no geographic variation in this ratio, although there is a seasonal variation with the ratio increasing as, spawning approaches. It therefore appears that urogenital papilla length has taxonomic value in male nonparasitic lampreys, provided the specimens are collected in spawning condition. The female papilla is too small to be of use.     

Parasitism offers large rewards but carries high risks: Predicting parasitic strategies under different life history conditions in lampreys

The loss of parasitism in metazoan lineages is often seen as unlikely, but it has occurred in some lineages (e.g., leeches, lampreys). How and why parasitism is lost is aptly addressed by studying lampreys, because extant species include a range of feeding modes and parasitism has been lost repeatedly. An individual‐based model was developed to determine whether variations in survival and growth rates in the larval and juvenile stages could favour parasitic or nonparasitic strategies. A realization of the model for a Lampetra spp. population, a genus which includes parasitic and nonparasitic animals, indicated that both strategies could be successful. A different model realization of the nonparasitic species Lethenteron appendix also agreed with expectations, and only nonparasitic strategies were successful. Modelling anadromous Petromyzon marinus produced only parasitic animals, as expected, but suggested two different adult sizes should appear in the population, which has not been reported in the literature. Finally, a realization of an Ichthyomyzon castaneus population, known to be parasitic only, rarely selected for parasitism (c. 7% of model iterations), possibly because the population used to parameterize the model was unusual for the species. The results suggest that nonparasitic lineages in lampreys are common because parasitism, while offering better growth, also has lower survival. Additionally, nonparasitic species may be generated at different rates because growth and survival thresholds in the model favouring parasitism are close to observed estimates in some populations. Loss of parasitism can occur when life stages have different trade‐offs in growth and survivability.     

Low reproductive isolation and highly variable levels of gene flow reveal limited progress towards speciation between European river and brook lampreys

Ecologically based divergent selection is a factor that could drive reproductive isolation even in the presence of gene flow. Population pairs arrayed along a continuum of divergence provide a good opportunity to address this issue. Here, we used a combination of mating trials, experimental crosses and population genetic analyses to investigate the evolution of reproductive isolation between two closely related species of lampreys with distinct life histories. We used microsatellite markers to genotype over 1000 individuals of the migratory parasitic river lamprey (Lampetra fluviatilis) and freshwater‐resident nonparasitic brook lamprey (Lampetra planeri) distributed in 10 sympatric and parapatric population pairs in France. Mating trials, parentage analyses and artificial fertilizations demonstrated a low level of reproductive isolation between species even though size‐assortative mating may contribute to isolation. Most parapatric population pairs were strongly differentiated due to the joint effects of geographic distance and barriers to migration. In contrast, we found variable levels of gene flow between sympatric populations ranging from panmixia to moderate differentiation, which indicates a gradient of divergence with some population pairs that may correspond to alternative morphs or ecotypes of a single species and others that remain partially isolated. Ecologically based divergent selection may explain these variable levels of divergence among sympatric population pairs, but incomplete genome swamping following secondary contact could have also played a role. Overall, this study illustrates how highly differentiated phenotypes can be maintained despite high levels of gene flow that limit the progress towards speciation.     

Evolutionary history of lamprey paired species Lampetra fluviatilis (L.) and Lampetra planeri (Bloch) as inferred from mitochondrial DNA variation

A remarkable trend in the evolution of lampreys is the occurrence in most genera of 'paired species', in which the parasitic anadromous lampreys are believed to have given rise to nonparasitic freshwater resident populations. The present work examines the phylogeography of the European paired species Lampetra fluviatilis and Lampetra planeri, in an attempt to elucidate species pair evolutionary history. We studied sequence variation in cytochrome b and ATPase 6, 8 mitochondrial genes in 63 individuals from 21 localities of the paired species throughout their distribution range. Results from the phylogenetic and nested clade analyses were largely consistent, suggesting the existence of three major evolutionary lineages: lineage I and possibly lineage II are widespread throughout Europe, while the most ancestral lineage III is apparently restricted to the Iberian Peninsula. The high genetic diversity observed in the Iberian Peninsula is probably the result of refugial persistence and subsequent accumulation of variation over several ice ages, whereas the low levels of genetic diversity observed in central and northern Europe should reflect a rapid postglacial colonization. Results suggest that L. planeri originated within at least two distinct evolutionary lineages, rejecting the single origin hypothesis. The observed lack of taxa monophyly within lineage I may be the result of ongoing gene flow if the two taxa are alternate life-history forms of a single species. However, structure within lineage I is also consistent with the hypothesis of divergence of taxa after postglacial dispersion (around 2000 generations ago) with incomplete lineage sorting. Further testing of the alternative hypotheses is warranted.     

Contrasting population genetic structure among freshwater‐resident and anadromous lampreys: the role of demographic history,differential dispersal and anthropogenic barriers to movement

The tendency of many species to abandon migration remains a poorly understood aspect of evolutionary biology that may play an important role in promoting species radiation by both allopatric and sympatric mechanisms. Anadromy inherently offers an opportunity for the colonization of freshwater environments, and the shift from an anadromous to a wholly freshwater life history has occurred in many families of fishes. Freshwater‐resident forms have arisen repeatedly among lampreys (within the Petromyzontidae and Mordaciidae), and there has been much debate as to whether anadromous lampreys, and their derived freshwater‐resident analogues, constitute distinct species or are divergent ecotypes of polymorphic species. Samples of 543 European river lamprey Lampetra fluviatilis (mostly from anadromous populations) and freshwater European brook lamprey Lampetra planeri from across 18 sites, primarily in the British Isles, were investigated for 13 polymorphic microsatellite DNA loci, and 108 samples from six of these sites were sequenced for 829 bp of mitochondrial DNA (mtDNA). We found contrasting patterns of population structure for mtDNA and microsatellite DNA markers, such that low diversity and little structure were seen for all populations for mtDNA (consistent with a recent founder expansion event), while fine‐scale structuring was evident for nuclear markers. Strong differentiation for microsatellite DNA loci was seen among freshwater‐resident L. planeri populations and between L. fluviatilis and L. planeri in most cases, but little structure was evident among anadromous L. fluviatilis populations. We conclude that postglacial colonization founded multiple freshwater‐resident populations with strong habitat fidelity and limited dispersal tendencies that became highly differentiated, a pattern that was likely intensified by anthropogenic barriers.     

The taxonomy of the Lampreys Geotria and Mordacia and their distribution in Australia

The taxonomy of the Southern Hemisphere lampreys, Qeotria and Mordacia , is reviewed. Many invalid species have been created within these genera due to a lack of knowledge of the great morphological changes that take place during development. The sequence of changes in the dentition of Mordacia is described in detail.
Geotria is now considered to be monotypic, containing only Q. australis Gray, which is found in Australia, New Zealand, and South America. Caragola is regarded as a synonym of Mordacia , and thus the exclusively South American C. lapicida becomes M. lapicida (Gray). The other Mordacia species, M. mordax (Richardson) and M. praecox Potter, are found only in Australia. All these species are anadromous and parasitic, except M. praecox , which is nonparasitic and never leaves fresh-water.
A comparison of anatomical features indicates that living lampreys (Petromyzonidae) are best separated into three subfamilies: Petromyzoninae to contain all Northern Hemisphere genera, Geotriinae for Geotria , and Mordaciinae for Mordacia.
A record of the Australian rivers in which lampreys have been found, shows that both genera are sympatric in South Australia, western Victoria, and Tasmania, and that only Qeotria is found in Western Australia, and only Mordacia in south-eastern Australia.     

Post‐zygotic hybrid viability in sympatric species pairs: a case study from European lampreys

Ecological speciation mechanisms are widely assumed to play an important role in the early stages of divergence between incipient species, and this especially true of fishes. In the present study, we tested explicitly for post‐zygotic barriers to gene flow between a sympatric, recently diverged lamprey species pair that likely arose through ecological divergence. Experimental in vitro hybridization between anadromous parasitic Lampetra fluviatilis and resident nonparasitic Lampetra planeri resulted in a high proportion of embryos capable of attaining the burrowing pro‐larval stage, strongly indicating no post‐zygotic barriers to gene flow between these species. A sympatric, locally‐adapted resident parasitic form of L. fluviatilis was also found to successfully hybridize with both members of this species pair. The consequences of these findings are discussed in the context of lamprey speciation. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 108 , 378–383.     

Metamorphosis of the mountain brook lamprey Ichthyomyzon greeleyi

Synopsis Metamorphosis of the nonparasitic mountain brook lamprey, I. greeleyi, is described within 7 phases based on external morphological changes. The commencement of metamorphosis in early August is consistent with the pattern for northern hemisphere lampreys which display an inverse relationship with latitude. The sequence of external changes including the development of eyes, oral disc, teeth, tongue, oral fimbriae and lateral line its consistent among individuals of I. greeleyi and lampreys in general. Some of the changes realized during metamorphosis of I. greeleyi are important to the adult period while others reflect their presumed parasitic ancestry. Energy reserves by nonfeeding I. greeleyi during the 104–140 days required to complete metamorphosis are replaced by water so that total length and body weight do not change significantly during this time.     

Social parasites among African allodapine bees (Hymenoptera,Anthophoridae, Ceratinini)*

Among the numerous nonparasitic allodapine bees there are 11 known species with parasitic or probably parasitic habits. These species live in nests of their close relatives, the female parasite replacing an egg-layer of the host. Seven of the parasitic species are distributed among four otherwise nonparasitic genera, while four species of parasites are placed in three exclusively parasitic genera. The parasites have mostly arisen independently from different nonparasitic forms. There is much convergence among the parasitic forms involving such characters as the flattened or concave face, reduced eyes, reduced mouthparts, reduced wing venation, and reduced pollen-carrying scopa. In the most specialized parasitic genera the mouthparts are so small as to be almost surely useless for obtaining food from flowers. Such bees must feed in the host nest, and are not found on flowers. Their wings must be adequate to take them to a new host nest but the reduced venation and eyes must reflect the reduced locomotary and sensory needs of a bee that does not visit flowers. In this paper a new, presumably parasitic Allodapula is described as is a parasitic Braunsapis, a parasitic Allodape, and a Eucondylops. A previously described Macrogalea is recognized as a parasite for the first time. A new genus and species of parasites Nasutapsis straussorum, allied to Braunsapis, is also described. All these forms are from Africa.     

Contemporary gene flow between “paired” silver (<Emphasis Type="Italic">Ichthyomyzon unicuspis</Emphasis>) and northern brook (<Emphasis Type="Italic">I. fossor</Emphasis>) lampreys: implications for conservation

In most lamprey genera, “paired” species exist in which the larvae are morphologically similar or indistinguishable but, following metamorphosis, one species becomes parasitic while the other bypasses the adult feeding phase and rapidly becomes sexually mature. Since DNA barcoding and similar studies using short segments of the mitochondrial genome do not provide sufficient resolution to distinguish between recent divergence and a lack thereof, the current study examined the relationship between the parasitic silver lamprey (Ichthyomyzon unicuspis) and nonparasitic northern brook lamprey (I. fossor) using up to 10,230 bp from the mitochondrial genome to make phylogenetic inferences and mitochondrial restriction fragment length polymorphism (RFLP) and microsatellite markers to test for significant differences in allele frequencies. We found that silver and northern brook lampreys are not reciprocally monophyletic; two lineages were observed but each occurred within both species. There also were no significant range-wide differences in RFLP haplotype or microsatellite allele frequencies between the species, nor were there significant differences where they occurred sympatrically within the Lake Huron basin. Significant genetic differentiation was found only within the Lake Michigan basin where the results were potentially confounded by geographic separation. Our results thus support suggestions that silver and northern brook lampreys represent ecotypes of a single species since, where they are sympatric, they appear to be experiencing ongoing gene flow. However, alternative life history strategies can be important for a species’ long-term persistence, and critical data are needed to decide whether these two feeding types should be managed as a single unit.     

Conservation status of Northern Hemisphere lampreys (Petromyzontidae)

Among the 34 nominal lamprey species in the Northern Hemisphere, ten are endangered; nine are vulnerable at least in part of their range, and one is extinct. The major cause is habitat degradation through pollution and stream regulation. Four conservation priorities are recommended: 1. The protection of all lamprey species or populations thereof listed as endangered; 2. where needed, the rehabilitation of the spawning streams of non-parasitic species and the removal or circumvention of any barriers preventing access to the spawning sites; 3. the protection of permanent freshwater resident populations of anadromous species, specifically of Entosphenus tridentatus, Lampetra ayresi, L. fluviatilis, Lethenteron japonicum and Petromyzon marinus : 4. the study of the conservation status of Asian lampreys.     

Quantitative studies on the skin of the paired species of lampreys,Lampetra fluviatilis (L.) and Lampetra planeri (BLOCH)

The number of mucous, club, and granular cells in the epidermis, and the number of rows of subcutaneous adipose cells, as well as the thickness of the epidermis and the dermal collagen layer, have been recorded for the larval and metamorphosing stages of the anadromous parasitic lamprey, Lampetra fluviatilis, and for the larval, metamorphosing, and adult stages of the nonparasitic lamprey, Lampetra planeri. In L. fluviatilis, the mucous cells predominated in all stages but were more abundant in fully metamorphosed individuals than in larvae. During metamorphosis, the number of granular cells increased continuously, whereas the club cells showed little change. Although lampreys do not feed during metamorphosis, there was an increase in the thickness of the epidermis and in the dermal collagen sheath; the latter increase probably foreshadows the increase in activity by the adults. Simultaneously, there is a reduction in the subcutaneous fat layer, which can be attributed to mobilization of lipid as an energy source. Changes similar to those just described for L. fluviatilis were also found in metamorphosing L. planeri. However, the pattern altered markedly during adult stages in this nonparasitic species. There were marked declines in the number of cells, in the thickness of the epidermis, in the width of the collagen sheath, and in the quantity of subcutaneous fat.     

An assessment of terminology for intraspecific diversity in fishes,with a focus on “ecotypes” and “life histories”

Understanding and preserving intraspecific diversity (ISD) is important for species conservation. However, ISD units do not have taxonomic standards and are not universally recognized. The terminology used to describe ISD is varied and often used ambiguously. We compared definitions of terms used to describe ISD with use in recent studies of three fish taxa: sticklebacks (Gasterosteidae), Pacific salmon and trout (Oncorhynchus spp., “PST”), and lampreys (Petromyzontiformes). Life history describes the phenotypic responses of organisms to environments and includes biological parameters that affect population growth or decline. Life‐history pathway(s) are the result of different organismal routes of development that can result in different life histories. These terms can be used to describe recognizable life‐history traits. Life history is generally used in organismal‐ and ecology‐based journals. The terms paired species/species pairs have been used to describe two different phenotypes, whereas in some species and situations a continuum of phenotypes may be expressed. Our review revealed overlapping definitions for race and subspecies, and subspecies and ecotypes. Ecotypes are genotypic adaptations to particular environments, and this term is often used in genetic‐ and evolution‐based journals. “Satellite species” is used for situations in which a parasitic lamprey yields two or more derived, nonparasitic lamprey species. Designatable Units, Evolutionary Significant Units (ESUs), and Distinct Population Segments (DPS) are used by some governments to classify ISD of vertebrate species within distinct and evolutionary significant criteria. In situations where the genetic or life‐history components of ISD are not well understood, a conservative approach would be to call them phenotypes.

The terminology used to describe intraspecific diversity is varied and often used ambiguously. “Ecotype” was originally used to describe patterns in genes and ecology, and recent studies employing this term tend to report a genetic basis in ISD. By contrast, “life history” describes biological parameters that affect demography, and this term tends to be used in organismal‐ and ecology‐based journals.     

Structure and pigmentation of tongue precursor of larval arctic lamprey Lethenteron camtschaticum (Petromyzontiformes, Petromyzontidae) from rivers of the Russian Far East

Systematics of adult lampreys based on the “paired species” concept divides anadromous and residential specimens mostly on the size and size-depended criteria. Larvae of the paired species are poorly distinguished, so scientists keep looking for new diagnostic features. In the present paper structure and coloration of the tongue precursor in Arctic lamprey, Lethenteron camtschaticum, from the watersheds of the Russian Far East, including the species type locality are discussed. The data show that use of Tongue Precursor Pigmentation as a key for species identification is premature because tongue precursor within species inhabiting one river system or the same region demonstrates all types of coloration. Structure of tongue precursor changes from triangular into bulbous during growth.