Genetic polymorphism in dopamine receptor D4 is associated with early body condition in a large population of greater flamingos,Phoenicopterus roseus

Body condition is an important determinant of fitness in many natural populations. However, as for many fitness traits, the underlying genes that regulate body condition remain elusive. The dopamine receptor D4 gene (DRD4) is a promising candidate as dopamine is known to play an important role in the regulation of food intake and the metabolism of both glucose and lipids in vertebrates. In this study, we take advantage of a large data set of greater flamingos, Phoenicopterus roseus, to test whether DRD4 polymorphism predicts early body condition (EBC) while controlling for whole-genome effects of inbreeding and outbreeding using microsatellite multilocus heterozygosity (MLH). We typed 670 o…

Overestimation of the strength of size-assortative pairing in taxa with cryptic diversity: a case of Simpson's paradox.

5 pages; International audience; Size-assortative pairing is one of the most common pairing patterns observed in nature and it probably occurs in many taxa with cryptic diversity. Observed patterns of size-assortative pairing in natural populations may thus be influenced by the co-occurrence of noninterbreeding cryptic groups of individuals living in sympatry. To quantify this potential bias, we sampled amphipods from the Gammarus pulex/Gammarus fossarum crustacean species complex in rivers containing two sympatric and morphologically cryptic groups, i.e. molecular operational taxonomic units (MOTUs). Within each river, MOTUs did not interbreed and differed in mean body size. We measured th…

Isolation and characterization of 8 microsatellite loci for the "killer shrimp'', an invasive Ponto-Caspian amphipod Dikerogammarus villosus (Crustacea: Amphipoda).

5 pages; International audience; Dikerogammarus villosus is a freshwater amphipod of the Ponto-Caspian origin recognized as one of the 100 worst alien species in Europe, having negative impact on biodiversity and functioning of the invaded aquatic ecosystems. The species has a wide ecophysiological tolerance and during the last 20 years it has rapidly spread throughout European inland waters. In consequence, it presents a major conservation management problem. We describe eight polymorphic microsatellite loci developed for D. villosus by combining a biotin-enrichment protocol and new generation 454GS-FLX Titanium pyrosequencing technology. When genotyped in 64 individuals from two locations…

Phylogeographic analysis of the red seaweed Palmaria palmata reveals a Pleistocene marine glacial refugium in the English Channel

Phylogeography has provided a new approach to the analysis of the postglacial history of a wide range of taxa but, to date, little is known about the effect of glacial periods on the marine biota of Europe. We have utilized a combination of nuclear, plastid and mitochondrial genetic markers to study the biogeographic history of the red seaweed Palmaria palmata in the North Atlantic. Analysis of the nuclear rDNA operon (ITS1-5.8S-ITS2), the plastid 16S-trnI-trnA-23S-5S, rbcL-rbcS and rpl12-rps31-rpl9 regions and the mitochondrial cox2-3 spacer has revealed the existence of a previously unidentified marine refugium in the English Channel, along with possible secondary refugia off the southwes…

Rapid range extension of the Ponto-Caspian amphipod Dikerogammarus villosus in France: potential consequences

Non-indigenous species are increasingly recognized as altering local com- munities in newly colonized areas. In some north European freshwater systems, the Ponto-Caspian invasive crustacean Dikerogammarus villosus (Amphipoda) is im- plicated to have such an effect, with general monitoring of its progress and general im- pact required. The present study contributes to this monitoring. D. villosus was ob- served in 2003 in all the major French rivers prospected (i.e. Rhine, Meuse, Moselle, Sao ne, Rho ne, Seine, and Loire), a European region previously overlooked for its co- lonization. This species was also detected in some tributaries of the rivers Sao ne and Seine, and in Geneva Lake. The …

Molecular markers for systematic identification and population genetics of the invasive Ponto-Caspian freshwater gammarid Dikerogammarus villosus (Crustacea, Amphipoda).

The Ponto-Caspian amphipod, Dikerogammarus villosus, is an invasive species of many European rivers. First, we show that size difference of nrDNA ITS1 allows discriminating D. villosus from Dikerogammarus bispinosus, a closely related but morphologically hardly distinguishable species. Second, we present two types of polymorphic markers for D. villosus, three microsatellites and two single nucleotide polymorphisms (SNPs) of mtDNA COI gene, which were scored by polymerase chain reaction-single strand conformational polymorphism (PCR-SSCP). These markers will be very useful in studying population genetics of D. villosus.

A co-invasive microsporidian parasite that reduces the predatory behaviour of its host Dikerogammarus villosus (Crustacea, Amphipoda).

SUMMARYParasites are known to affect the predatory behaviour or diet of their hosts. In relation to biological invasions, parasites may significantly influence the invasiveness of the host population and/or mediate the relationships between the invader and the invaded community. Dikerogammarus villosus, a recently introduced species, has had a major impact in European rivers. Notably, its high position in trophic web and high predatory behaviour, have both facilitated its invasive success, and affected other macroinvertebrate taxa in colonized habitats. The intracellular parasite Cucumispora dikerogammari, specific to D. villosus, has successfully dispersed together with this amphipod. Data…

Cryptic diversity within three South American whip spider species (Arachnida, Amblypygi)

4 pages; International audience; Cryptic diversity (CD), the presence of highly divergent phylogenetic lineages within closed morphological species, has been documented for many taxa. Great arachnid orders such as Araneae or Scorpiones are well studied and many cases of CD have been described therein; to date, however, related research on smaller arachnid orders, such as whip spiders (Amblypygi), remains lacking. In the current study, we investigated CD based on cytochrome oxidase 1 (COI) in three nominal species of the genus Heterophrynus (H. alces, H. batesii, and H. longicornis), represented by 65 specimens. The sequences were compared using three different methods. All three species sho…

Confrontation of cryptic diversity and mate discrimination within Gammarus pulex and Gammarus fossarum species complexes.

16 pages; International audience; Freshwater amphipods Gammarus fossarum and Gammarus pulex are widespread in Europe, with some evidence of cryptic diversity in the former. We used DNA barcoding to assess genetic diversity within and among amphipod populations and examined mate discrimination and pre-copulatory pair formation between genetically divergent individuals. Eight distinct G. fossarum and four distinct G. pulex molecular operational taxonomic units (MOTUs) were detected. Among the 33 amphipod populations sampled, 11 contained a single MOTU, 11 had two and 11 were composed of three sympatric MOTUs. Genetic divergences between sympatric MOTUs (G. fossarum and G. pulex MOTUs combined…

Cucumispora dikerogammari n. gen. (Fungi: Microsporidia) infecting the invasive amphipod Dikerogammarus villosus: a potential emerging disease in European rivers.

SUMMARYDikerogammarus villosusis an invasive amphipod that recently colonized the main rivers of Central and Western Europe. Two frequent microsporidian parasites were previously detected in this species, but their taxonomic status was unclear. Here we present ultrastructural and molecular data indicating that these two parasites are in fact a single microsporidian species. This parasite shares numerous characteristics ofNosemaspp. It forms elongate spores (cucumiform), developing in direct contact with host cell cytoplasm; all developmental stages are diplokaryotic and the life cycle is monomorphic with disporoblastic sporogony. Initially this parasite was described asNosema dikerogammariO…

Morphological vs. molecular delineation of taxa across montane regions in Europe: the case study of Gammarus balcanicus Schäferna, (Crustacea: Amphipoda)

Mountainous areas are characterized by substantial biodiversity and endemicity due to their complex geological history and habitat fragmentation. Hence, it can be assumed that particularly high species richness can be found in organisms with limited dispersal capabilities that inhabit mountain streams. A number of scientific papers focus on molecular phylogeography or traditional taxonomy of species or species groups inhabiting such habitats. However, there is a lack of studies that integrate morphological and molecular data to identify and delineate cryptic species. For practical reasons, uncovering cryptic diversity is crucial in taxa used in biomonitoring. Distinct species, hard to separ…

Neogene paleogeography provides context for understanding the origin and spatial distribution of cryptic diversity in a widespread Balkan freshwater amphipod

BackgroundThe Balkans are a major biodiversity and endemism hotspot, worldwide. Among the freshwater biota, amphipods are known for their high cryptic diversity. However, little is known about the temporal and paleogeographic aspects of their evolutionary history. We used paleogeography as a framework for understanding the onset of diversification inGammarus roeselii: (1) we hypothesised that, given the high number of isolated waterbodies in the Balkans, the species is characterised by high level of cryptic diversity, even on a local scale; (2) the long geological history of the region might promote pre-Pleistocene divergence between lineages; (3) given thatG. roeseliithrives both in lakes …

Evidence for an Association between Post-Fledging Dispersal and Microsatellite Multilocus Heterozygosity in a Large Population of Greater Flamingos

10 pages; International audience; DISPERSAL CAN BE DIVIDED INTO THREE STAGES: departure, transience and settlement. Despite the fact that theoretical studies have emphasized the importance of heterozygosity on dispersal strategies, empirical evidence of its effect on different stages of dispersal is lacking. Here, using multi-event capture-mark-recapture models, we show a negative association between microsatellite multilocus heterozygosity (MLH; 10 loci; n = 1023) and post-fledging dispersal propensity for greater flamingos, Phoenicopterus roseus, born in southern France. We propose that the negative effects of inbreeding depression affects competitive ability and therefore more homozygous…

Out of the Black Sea: phylogeography of the invasive killer shrimp Dikerogammarus villosus across Europe.

20 pages; International audience; The amphipod Dikerogammarus villosus has colonized most of the European main inland water bodies in less than 20 years, having deteriorating effect on the local benthic communities. Our aim was to reveal the species phylogeography in the native Black Sea area, to define the source populations for the colonization routes in continental Europe and for the newly established UK populations. We tested for the loss of genetic diversity between source and invasive populations as well as along invasion route. We tested also for isolation by distance. Thirty three native and invasive populations were genotyped for mtDNA (COI, 16S) and seven polymorphic nuclear micro…

Tracking zoonotic pathogens using blood-sucking flies as 'flying syringes'

About 60% of emerging infectious diseases in humans are of zoonotic origin. Their increasing number requires the development of new methods for early detection and monitoring of infectious agents in wildlife. Here, we investigated whether blood meals from hematophagous flies could be used to identify the infectious agents circulating in wild vertebrates. To this aim, 1230 blood-engorged flies were caught in the forests of Gabon. Identified blood meals (30%) were from 20 vertebrate species including mammals, birds and reptiles. Among them, 9% were infected by different extant malaria parasites among which some belonged to known parasite species, others to new parasite species or to parasite …

The ‘killer shrimp’Dikerogammarus villosus(Crustacea, Amphipoda) invading Alpine lakes: overland transport by recreational boats and scuba-diving gear as potential entry vectors?

The alien freshwater amphipod of Ponto-Caspian origin, Dikerogammarus villosus, also known as the killer shrimp, is recognized as being one of the worst invasive alien species in Europe, representing a major conservation problem. Recently, the species has been reported to invade lakes in the Alps in putative association with overland transport linked with recreational activities. This study provided a method to assess risk associated with this overland transport and an opportunity to set up a rationale for effective preventive conservation management. A field survey of 60 lakes encompassing all the Alpine area has revealed the presence of killer shrimp in 12 lakes. Subsequent multivariate d…

Invasion de Dikerogammarus villosus (Crustacé, Amphipode) dans les eaux continentales françaises : dynamiques et conséquences

National audience

Permanent Genetic Resources added to Molecular Ecology Resources Database 1 October 2009–30 November 2009.

5 pages; International audience; This article documents the addition of 411 microsatellite marker loci and 15 pairs of Single Nucleotide Polymorphism (SNP) sequencing primers to the Molecular Ecology Resources Database. Loci were developed for the following species: Acanthopagrus schlegeli, Anopheles lesteri, Aspergillus clavatus, Aspergillus flavus, Aspergillus fumigatus, Aspergillus oryzae, Aspergillus terreus, Branchiostoma japonicum, Branchiostoma belcheri, Colias behrii, Coryphopterus personatus, Cynogolssus semilaevis, Cynoglossus semilaevis, Dendrobium officinale, Dendrobium officinale, Dysoxylum malabaricum, Metrioptera roeselii, Myrmeciza exsul, Ochotona thibetana, Neosartorya fisc…

The legacy of a vanished sea: a high level of diversification within a European freshwater amphipod species complex driven by 15 My of Paratethys regression.

16 pages; International audience; The formation of continental Europe in the Neogene was due to the regression of the Tethys Ocean and of the Paratethys Sea. The dynamic geology of the area and repetitious transitions between marine and freshwater conditions presented opportunities for the colonization of newly emerging hydrological networks and diversification of aquatic biota. Implementing mitochondrial and nuclear markers in conjunction with a large-scale sampling strategy, we investigated the impact of this spatiotemporal framework on the evolutionary history of a freshwater crustacean morphospecies. The Gammarus balcanicus species complex is widely distributed in the area previously oc…

Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans

Several parasite species have the ability to modify their host's phenotype to their own advantage thereby increasing the probability of transmission from one host to another. This phenomenon of host manipulation is interpreted as the expression of a parasite extended phenotype. Manipulative parasites generally affect multiple phenotypic traits in their hosts, although both the extent and adaptive significance of such multidimensionality in host manipulation is still poorly documented. To review the multidimensionality and magnitude of host manipulation, and to understand the causes of variation in trait value alteration, we performed a phylogenetically corrected meta-analysis, focusing on a…

Highly contrasted population genetic structures in a host-parasite pair in the Caribbean Sea.

Evolution and population genetic structure of marine species across the Caribbean Sea are shaped by two complex factors: the geological history and the present pattern of marine currents. Characterizing and comparing the genetic structures of codistributed species, such as host–parasite associations, allow discriminating the relative importance of environmental factors and life history traits that influenced gene flow and demographic events. Using microsatellite and Cytochrome Oxidase I markers, we investigated if a host–parasite pair (the heart urchin Meoma ventricosa and its parasitic pea crab Dissodactylus primitivus) exhibits comparable population genetic structures in the Caribbean Sea…

Microsporidian disease of the invasive amphipod Dikerogammarus villosus and the potential for its transfer to local invertebrate fauna.

12 pages; International audience; Invasive species may introduce novel pathogens to a colonised area. Most of the time emerging pathogens are detected a posteriori, but recognition of a priori emergence of an invasive disease by host shift may be useful for predictive purposes. Here, we studied if the microsporidian parasite Cucumispora dikerogammari infecting the invasive Ponto-Caspian amphipod Dikerogammarus villosus, has the potential to become an emergent disease in invaded rivers in Western and Central Europe. We first showed that this parasite decreases the survival of D. villosus in the later stages of infection development. However, the host reproduces earlier in response to the inf…

Heterozygosity-fitness correlations in adult and juvenile Zenaida Dove, Zenaida aurita.

10 pages; International audience; Understanding how fitness is related to genetic variation is of crucial importance in both evolutionary ecology and conservation biology. We report a study of heterozygosity-fitness correlations in a wild, noninbred population of Zenaida Doves, Zenaida aurita, based on a sample comprising 489 individuals (382 adults and 107 juveniles) typed at 13 microsatellite loci, resulting in a data set comprising 5793 genotypes. In both adults and juveniles, and irrespective of sex, no evidence was found for an effect of either multilocus or single-locus heterozygosity on traits potentially related to fitness such as foraging tactic, competitive ability, and fluctuatin…

Colonisation and diversification of the Zenaida dove (Zenaida aurita) in the Antilles: phylogeography, contemporary gene flow and morphological divergence.

12 pages; International audience; Caribbean avifaunal biogeography has been mainly studied based on mitochondrial DNA. Here, we investigated both past and recent island differentiation and micro-evolutionary changes in the Zenaida Dove (Zenaida aurita) based on combined information from one mitochondrial (Cytochrome c Oxydase subunit I, COI) and 13 microsatellite markers and four morphological characters. This Caribbean endemic and abundant species has a large distribution, and two subspecies are supposed to occur: Z. a. zenaida in the Greater Antilles (GA) and Z. a. aurita in the Lesser Antilles (LA). Doves were sampled on two GA islands (Puerto Rico and the British Virgin Islands) and six…

First breeding evidence of marbled duck (Marmaronetta angustirostris) in Libya.

4 pages; International audience; The first evidence of breeding of Marbled Duck (Marmaronetta angustirostris) in Libya, North Africa, is reported. In June 2012, at Mallaha wetland, in Tripoli, Libya, two dead ducklings were found that were later genetically identified as Marbled Duck. This breeding evidence suggests that this and other duck species may breed elsewhere in Libya. Better knowledge on Libyan, and more generally on north African, waterbirds is needed to document the population size and the status of these species. Such information will be important to secure the future of threatened species, such as the Marbled Duck.

The killer shrimp, Dikerogammarus villosus, invading European Alpine lakes: a single main source but independent founder events with an overall loss of genetic diversity.

16 pages; International audience; 1. The effects of biological invasions are generally more detrimental in isolated ecosystems than in the interconnected ones and freshwater lakes appear to be particularly fragile. The Ponto-Caspian freshwater amphipod Dikerogammarus villosus (Pontogammaridae), also known as the killer shrimp, is a highly invasive species that can have significant ecological impacts on receiving ecosystems. It has colonised most of the European main inland waterbodies, including at least 12 lakes in the Alps – an area of high conservational priority and, at the same time, heavily affected by anthropogenic changes. Particularly, overland translocations of boats among tourist…

Territoriality versus flocking in the Zenaida dove (Zenaida aurita): resource polymorphism revisited using morphological and genetic analyses.

11 pages; International audience; The term “resource polymorphism” refers to the existence of alternative phenotypes in relation to resource use, as a result of disruptive selection. Evidence for resource polymorphism is widespread in fish but remains scarce in birds. Although Zenaida Doves (Zenaida aurita) usually defend year-round territories, doves on Barbados can also be observed foraging at seed-storage sites in large flocks with little, if any, inter-individual aggression. On the basis of morphological variation, it has been suggested (Sol et al. 2005) that this represents a case of resource polymorphism, primarily driven by competition for territories. Using new data, we revisited th…

Genetic evidence confirms polygamous mating system in a crustacean parasite with multiple hosts.

Mating systems are diverse in animals, notably in crustaceans, but can be inferred from a limited set of parameters. Baeza and Thiel (2007) proposed a model predicting mating systems of symbiotic crustaceans with three host characteristics and the risk of predation. These authors proposed five mating systems, ranging from monogamy to polygynandry (where multiple mating occurs for both genders). Using microsatellite loci, we tested the putatively mating system of the ectoparasite crab Dissodactylus primitivus. We determined the mating frequencies of males and females, parentage assignment (COLONY & GERUD software) as well as the contents of female spermathecae. Our results are globally consi…

An integrative approach challenges species hypotheses and provides hints for evolutionary history of two Mediterranean freshwater palaemonid shrimps (Decapoda: Caridea).

25 pages; International audience; The Mediterranean Region is a biodiversity/endemism hotspot whose freshwater fauna remains largely unexplored. Our integrative study challenges the taxonomic status of two freshwater palaemonid shrimps, Palaemon antennarius and Palaemon minos. Three molecular operational taxonomic units (MOTUs) were defined based on 352 cytochrome oxidase subunit I (COI) sequences and 88 haplotypes. Two belonged to P. antennarius: one inhabiting the Apennine Peninsula and Sicily, and the other from the Balkan Peninsula. Palaemon minos was the third MOTU, found on Crete. The Balkan MOTU of P. antennarius was genetically closer to P. minos than to the other conspecific MOTU. …

Extension rapide de l'aire de répartition de Dikerogammarus villosus (Crustacé, Amphipode) en France : Causes et conséquences

International audience

Is the host or the parasite the most locally adapted in an amphipod–acanthocephalan relationship? A case study in a biological invasion context

8 pages; International audience; Manipulative endoparasites with complex life cycles can alter their intermediate host immunity and behaviour in ways that increase survival probability within the host body cavity and enhance successful transmission to the definitive host. These parasitic manipulations are variable among and within parasite species and may result from co-evolutionary processes, in which the parasite is constrained for adaptation to the local intermediate host. Hence, arrival of a new host species in a local host population may promote local parasite maladaptation. This study tested the occurrence of local adaptation in two distantly located populations of the acanthocephalan…

Author response: Tracking zoonotic pathogens using blood-sucking flies as 'flying syringes'

Levels of genetic differentiation and gene flow between four populations of the Scaly-naped Pigeon, Patagioenas squamosa : implications for conservation

Island-endemic columbid species are particularly vulnerable to environmental degradation, extreme climatic events, and interactions with exotic species. The situation might be even more critical in the case of exploited species, where legal hunting and poaching can severely affect population dynamics. Here we document for the first time the genetic structure of the Scaly-naped Pigeon, Patagioenas squamosa, a Caribbean-endemic columbid species of cynegetic interest, over a large part of its range. Using both mitochondrial DNA and nuclear markers (microsatellites), we investigated gene flow, genetic diversity, and genetic structure among four islands populations originating from Puerto-Rico, …

Data from: Evidence for an association between post-fledging dispersal and microsatellite multilocus heterozygosity in a large population of greater flamingos

Dispersal can be divided into three stages: departure, transience and settlement. Despite the fact that theoretical studies have emphasized the importance of heterozygosity on dispersal strategies, empirical evidence of its effect on different stages of dispersal is lacking. Here, using multi-event capture-mark-recapture models, we show a negative association between microsatellite multilocus heterozygosity (MLH; 10 loci; n = 1023) and post-fledging dispersal propensity for greater flamingos, Phoenicopterus roseus, born in southern France. We propose that the negative effects of inbreeding depression affects competitive ability and therefore more homozygous individuals are more likely to di…