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.     

Polymorphism of spawners of the resident form of European river lamprey <Emphasis Type="Italic">Lampetra fluviatilis</Emphasis> (Petromyzontidae)

Data on polymorphism (plastic and meristic characters) are obtained for spawners of resident nonparasitic form of European river lamprey Lampetra fluviatilis from the Serebristaya River. The new data verify the diagnosis of this species and contribute to the formulation of a hypothesis on the presence of several phenotypic groups: dwarf, small-sized, and common. Analysis of plastic characters and of the number of trunk myomeres demonstrated that the values of these characters reliably depend on position of lampreys in a certain discerned group. Some aspects of biology of this species are discussed: spawning and interaction between resident nonparasitic river and migrating parasitic lampreys.     

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.     

Repeated origins of social parasitism in allodapine bees indicate that the weak form of Emery's rule is widespread,yet sympatric speciation remains highly problematic

The evolutionary origins of social parasitism are very unevenly distributed among ants, bees and wasps, but social parasite lineages are frequently close relatives of their host lineages. Two explanations for these relationships have been proposed: (1) initially, social species are more likely to become parasitic on relatively closely related social species, because they share life history, physiological and behavioural traits that allow successful integration within the host colony; and (2) social parasites have evolved directly from their host lineage via sympatric speciation. Comparative approaches, covering multiple origins and intermediate evolutionary stages, are needed to determine which of these possibilities is more likely. We use molecular phylogenetics to examine multiple origins of parasitism in the bee tribe Allodapini. We identify seven origins resulting in obligate social parasitism (inquilinism), one origin of facultative social parasitism, which was followed by subsequent speciation and where both daughter species remained facultatively parasitic, and one case of frequent facultative heterospecific co‐nesting that probably represents incipient social parasitism. All host–parasite lineage pairs show strong phylogenetic affinities, but only the case of facultative heterospecific nesting involves true sister species relationships. Our results are consistent with the range of parasitic relationships that are expected under an allopatric model for the origin of social parasitism, but are highly problematic for a sympatric speciation model. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 320–331.     

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.     

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.     

Diet specialization and brood parasitism in cuckoo species

1. Brood parasitism is a breeding strategy adopted by many species of cuckoos across the world. This breeding strategy influences the evolution of life histories of brood parasite species.
2. In this study, we tested whether the degree on diet specialization is related to the breeding strategy in cuckoo species, by comparing brood parasite and nonparasite species. We measured the gradient of diet specialization of cuckoos, by calculating the Gini coefficient, an index of inequality, on the multiple traits describing the diet of species. The Gini coefficient is a measure of statistical dispersion on a scale between 0 and 1, reflecting a gradient from low to high specialization, respectively. First, we tested the strength of the phylogenetic signal of diet specialization index among cuckoo species worldwide. Then, we ran phylogenetic generalized least square (PGLS) models to compare diet specialization, distribution range, and body mass of parasitic and nonparasitic cuckoo species, considering the phylogenetic signal of data.
3. After adjusting for the phylogenetic signal of the data and considering both, species distribution range and species body mass, brood parasitic cuckoos were characterized by higher diet specialization than nonbrood parasitic species. Brood parasitic species were also characterized by a larger breeding distribution range than nonparasitic species.
4. The findings of this study provide an additional understanding of the cuckoos’ ecology, relating diet and breeding strategies, information that could be important in conservation ecology.

     

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.     

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.     

Rapid laying by Brown-headed Cowbirds Molothrus ater and other parasitic birds

We compared the length of time parasitic and nonparasitic female birds spent on nests while laying eggs (laying bouts) to evaluate the hypothesis that rapid laving by parasitic Brown-headed Cowbirds Molothrus ater and other parasitic birds is a specialization for brood parasitism. Brown-headed Cowbirds typically spent less than 1 min on host nests while laying (41.0 ± 4.58 [mean ± s.e.] s, n = 21). In contrast, mean laving bouts of six nonparasitic icterine species ranged from 21.5 min to 53.4 min, and laying bouts of 13 other passerine species ranged from 20.7 min to 103.7 min. By spending only a few seconds on the nest while laying, brood parasites probably increase their chances of parasitizing nests unnoticed by hosts or, if noticed, are harassed by hosts for less time. Rapid laying may be adaptive if aggression by hosts can thwart attempted parasitism by chasing away the parasite, preventing the parasite from entering the nest or injuring the parasite. Rapid laying may increase the likelihood that the parasitic egg will be accepted. We tested some of these hypotheses by recording the responses of three frequently parasitized species to a stuffed female cowbird placed on their nests for 1 min. All species attacked the model vigorously; however, the mean time for discovery of the model ranged from 3 min to 17 min, ample time for female cowbirds to parasitize the nests. We concluded that rapid laying by parasitic birds is an adaptation for parasitism and, in Brown-headed Cowbirds, reduces the chances that the parasite will be attacked by hosts.     

The effect of relaxed functional constraints on the photosynthetic gene rbcL in photosynthetic and nonphotosynthetic parasitic plants

The photosynthetic gene rbcL has been lost or dramatically altered in some lineages of nonphotosynthetic parasitic plants, but the dynamics of these events following loss of photosynthesis and whether rbcL has sustained functionally significant changes in photosynthetic parasitic plants are unknown. To assess the changes to rbcL associated with the loss of functional constraints for photosynthesis, nucleotide sequences from nonparasitic and parasitic plants of Scrophulariales were used for phylogeny reconstruction and character analysis. Plants in this group display a broad range of parasitic abilities, from photosynthetic ("hemiparasites") to nonphotosynthetic ("holoparasites"). With the exception of Conopholis (Orobanchaceae), the rbcL locus is present in all parasitic plants of Scrophulariales examined. Several holoparasitic genera included in this study, including Boschniakia, Epifagus, Orobanche, and Hyobanche, have rbcL pseudogenes. However, the holoparasites Alectra orobanchoides, Harveya capensis, Harveya purpurea, Lathraea clandestina, Orobanche corymbosa, O. fasciculata, and Striga gesnerioides have intact open reading frames (ORFs) for the rbcL gene. Phylogenetic hypotheses based on rbcL are largely in agreement with those based on sequences of the nonphotosynthetic genes rps2 and matK and show a single origin of parasitism, and loss of photosynthesis and pseudogene formation have been independently derived several times in Scrophulariales. The mutations in rbcL in nonparasitic and hemiparasitic plants would result in largely conservative amino acid substitutions, supporting the hypothesis that functional proteins can experience only a limited range of changes, even in minimally photosynthetic plants. In contrast, ORFs in some holoparasites had many previously unobserved missense substitutions at functionally important amino acid residues, suggesting that rbcL genes in these plants have evolved under relaxed or altered functional constraints.      

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.     

Molecular genetic perspectives on avian brood parasitism

Advances in molecular genetic techniques have provided new approachesfor addressing evolutionary questions about brood parasiticbirds. We review recent studies that apply genetic data to thesystematics, population biology, and social systems of avianbrood parasites and suggest directions for future research.Recent molecular systematics studies indicate that obligatebrood parasitism has evolved independently in seven differentavian lineages, a tally that has increased by one in cuckoos(Cuculiformes) and decreased by one in passeriforms (Passeriformes)as compared to conventional taxonomy. Genetic parentage analysessuggest that brood parasitic birds are less promiscuous thanmight be expected given their lack of nesting and parental carebehavior. Host-specificity in brood parasites, which has importantimplications for host-parasite coevolution, has been evaluatedusing both population genetic and parentage analyses. Femalelineages are faithful to particular host species over evolutionarilysignificant time scales in both common cuckoos (Cuculus canorus)and indigobirds (Vidua spp.), but differences in the host-specificityof male parasites has resulted in different patterns of diversificationin these two lineages. Future research on brood parasitism willbenefit from the availability of comprehensive molecular phylogeniesfor brood parasites and their hosts and from advances in functionalgenomics.     

Loss of larval parasitism in parasitengonine mites

Larval Parasitengona are typically parasites, yet at least 29 species of water mites and one species of Trombidiidae forgo larval feeding and any association with a host. Species with non-feeding larvae are isolated cases within species groups or genera where the remaining species have parasitic larvae. Species without larval parasitism occur in at least 14 genera, eight families and four superfamilies of water mites; the loss of larval parasitism is presumably polyphyletic, having occurred at least 21 times. Lineages of water mites with non-feeding larvae frequently exist in parallel with almost identical populations or species that have parasitic larvae. Thus, there is tremendous potential for studies comparing the relative merits of the two life history strategies. Comparisons indicate that adults from lineages with non-parasitic larvae produce smaller numbers of larger eggs; the extra nutrition included in larger eggs permits the larvae to forgo feeding. Non-feeding larvae frequently have wider dorsal plates but reduced leg length, setal length and sclerotization when compared to parasitic larvae from sister lineages. The adults of lineages with non-feeding larvae are frequently smaller in comparison to adults of sister lineages with parasitic larvae. There is no apparent pattern in relation to habitat: lineages lacking larval parasitism occur in streams, temporary ponds and the littoral and planktonic regions of permanent lakes. © Rapid Science Ltd. 1998     

Variations in the presence of chloride cells in the gills of lampreys (Petromyzontiformes) and their evolutionary implications

Although confined to fresh water, non‐parasitic species of lampreys and the landlocked parasitic sea lamprey, all of which were derived relatively recently from anadromous ancestors, still develop chloride cells, whose function in their ancestors was for osmoregulation in marine waters during the adult parasitic phase. In contrast, such cells are not developed by the non‐parasitic least brook lamprey Lampetra aepyptera, which has been separated from its ancestor for >2 million years, nor by the freshwater parasitic species of the genus Ichthyomyzon. The length of time that a non‐parasitic species or landlocked parasitic form or species has spent in fresh water is thus considered the overriding factor determining whether chloride cells are developed by those lampreys.     

Metamorphic changes in the intestine of three species of lampreys

Measurements have been made of those changes which lead to increases in the surface area of the intestine during the metamorphosis of three species of lampreys. Although the intestine of the Southern Hemisphere lamprey, Geotria australis, increases in length by 1.13 times and in diameter by 1.12 times, the main factor influencing the 5.71 times increase in surface area is the development of longitudinal folds. The contribution of the typhlosole to the internal perimeter of the intestine is less in most life cycle stages of G. australis than in Lampetra spp. The changes in the various intestinal measurements of the nonparasitic species L. planeri parallel those of the presumed ancestral parasitic species, L. fluviatilis, during the first six stages of metamorphosis. However, the longitudinal folds, but not the typhlosole, subsequently start regressing in L. planeri just after the time when the rate of gonadal development increases markedly. An account is also given of the pattern of fold formation and the development of the typhlosolar vein in G. australis.     

On the origin and rarity of interspecific nest parasitism in birds

Interspecific nest parasitism is surprisingly rare in birds given the potential advantages for the parasite of exploiting the parental care of other species. One possibility is that chicks will not thrive with the parental care and food of heterospecifics. I simulated parasitism in nonparasitic congeners by switching eggs between nests of three species of titmice (great tit Parus major, blue tit Parus caeruleus, and coal tit Parus ater). The experiment showed that compatibility of parental care was not a constraint preventing parasitism. I also used the model system to compare fitness consequences of inter- and intraspecific nest parasitism, addressing the problem of which form is ancestral. Fledging success (body mass, survival) was higher when an egg was added to the nest of a smaller species than to the nest of a conspecific and also higher when the parasitic chick hatched early rather than late relative to host chicks. This suggests that interspecific nest parasitism may not require a stage of intraspecific nest parasitism before evolving but may start from a larger species directly exploiting the parental care of a smaller species or a species with shorter incubation period directly exploiting a species with longer incubation period.     

New insights into the population biology of endoparasitic Rafflesiaceae

Parasitic plants demonstrate a diversity of growth strategies, life histories, and developmental and physiological characteristics. Most research to date has focused on a narrow range of parasitic taxa, particularly in the Orobanchaceae, while the other independent origins of parasitism have largely gone unstudied. One type of parasite that has received relatively little attention are the endophytic parasites, which have a fascinating growth strategy where the parasite is embedded within the host tissue, with the flower the only externally visibly plant part. Endophytic growth makes it challenging to understand basic aspects of species biology, such as the size of a given parasite, the number of parasites per host, and the genetic diversity of populations. Recent studies by Barkman et al. (2017) and Pelser et al. (2017) have used microsatellite genotyping to investigate the population biology of endoparasitic Rafflesiaceae species in Asia. They show the potential for extensive parasite spread within a host vine and the strong partitioning of genetic diversity by host. These species are also shown to have an outcrossing mating system. However, these studies suggest different reproductive strategies, one supporting monoecy and one suggesting dioecy. Overall, these studies partly “lift the lid” on the cryptic biology of Rafflesia and the Rafflesiaceae and open the door for future comparative studies between endophytic and free-living parasitic plants.     

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.