Genetic analysis reveals the diversity of larval Gobiidae in a temperate estuary

Using molecular tools to examine Gobiidae, the second most abundant taxon in ichthyoplankton samples in the Gulf of Riga (Baltic Sea), the sand goby Pomatoschistus minutus was the most abundant taxon (82% of all individuals analysed), the common goby Pomatoschistus microps constituted 12% and the black goby Gobius niger 6%. The spatiotemporal distribution of P. microps and G. niger indicated a preference for habitats closer to the river inlet and their abundances increased slightly towards the end of the sampling period in summer. The species composition was interpreted in the context of the prevailing habitat conditions, characterized by extremely low water transparency, low salinity, limited spread of vegetated area and dominance of sandy–muddy substrata.     

Einnischung von fünf Grundeln (Teleostei, Gobiidae) der Ostsee und ihre Deutung mit Hilfe der Präadaptationstheorie

Niche occupation by 5 goby species (Teleostei, Gobiidae) in the Baltic Sea and its interpretation by means of the theory of pre-adaptation The habitats and prey of five goby species were investigated near the shore of the Lübeck Bight (SW Baltic) during the period 1989–1991. Observations showed that Gobius niger is a macrobenthos feeder, Pomatoschistus microps a meiobenthos feeder; Pomatoschistus pictus prefers meiobenthos as well as plankton while Pomatoschistus minutus feeds on benthos of every size, as well as planktonic cope-pods when offered in surplus; Gobiusculus flavescens is generally a plankton feeder but, when this component is in short supply in the summer, changes to macrobenthos. P. pictus and P. microps existed at different depths; G. flavescens and P. minutus presented countercurrent densities in shallow habitats during the course of a year. This adaptability of behaviour in habitat and prey choice can be explained by the modification ability of pre-adaptional genes in the goby genomes. After having invaded species-poor habitats such as the brackish Baltic Sea, wide niche dimensions are initially occupied. The niche is here considered to be an attribute of the species as well as of the habitat according to GÜNTHER (1950). Hence, innidation is defined as a process which implies specialization by loss of most preadaptations and leads to the optimal use of the ecosystem by the species. This process of a single species corresponds to the maturation of successions of whole biocoenoses.     

Spatiotemporal and gender‐specific parasitism in two species of gobiid fish

Parasitism is considered a major selective force in natural host populations. Infections can decrease host condition and vigour, and potentially influence, for example, host population dynamics and behavior such as mate choice. We studied parasite infections of two common marine fish species, the sand goby (Pomatoschistus minutus) and the common goby (Pomatoschistus microps), in the brackish water Northern Baltic Sea. We were particularly interested in the occurrence of parasite taxa located in central sensory organs, such as eyes, potentially affecting fish behavior and mate choice. We found that both fish species harbored parasite communities dominated by taxa transmitted to fish through aquatic invertebrates. Infections also showed significant spatiotemporal variation. Trematodes in the eyes were very few in some locations, but infection levels were higher among females than males, suggesting differences in exposure or resistance between the sexes. To test between these hypotheses, we experimentally exposed male and female sand gobies to infection with the eye fluke Diplostomum pseudospathaceum. These trials showed that the fish became readily infected and females had higher parasite numbers, supporting higher susceptibility of females. Eye fluke infections also caused high cataract intensities among the fish in the wild. Our results demonstrate the potential of these parasites to influence host condition and visual abilities, which may have significant implications for survival and mate choice in goby populations.     

Sperm adaptation in relation to salinity in three goby species

In externally fertilizing species, the gametes of both males and females are exposed to the influences of the environment into which they are released. Sperm are sensitive to abiotic factors such as salinity, but they are also affected by biotic factors such as sperm competition. In this study, the authors compared the performance of sperm of three goby species, the painted goby, Pomatoschistus pictus, the two-spotted goby, Pomatoschistus flavescens, and the sand goby, Pomatoschistus minutus. These species differ in their distributions, with painted goby having the narrowest salinity range and sand goby the widest. Moreover, data from paternity show that the two-spotted goby experiences the least sperm competition, whereas in the sand goby sperm competition is ubiquitous. The authors took sperm samples from dissected males and exposed them to high salinity water (31 PSU) representing the North Sea and low salinity water (6 PSU) representing the brackish Baltic Sea Proper. They then used computer-assisted sperm analysis to measure the proportion of motile sperm and sperm swimming speed 10 min and 20 h after sperm activation. The authors found that sperm performance depended on salinity, but there seemed to be no relationship to the species' geographical distribution in relation to salinity range. The species differed in the proportion of motile sperm, but there was no significant decrease in sperm motility during 20 h. The sand goby was the only species with motile sperm after 72 h.     

Surprising similarity of sneaking rates and genetic mating patterns in two populations of sand goby experiencing disparate sexual selection regimes

Molecular markers have proved extremely useful in resolving mating patterns within individual populations of a number of species, but little is known about how genetic mating systems might vary geographically within a species. Here we use microsatellite markers to compare patterns of sneaked fertilization and mating success in two populations of sand goby (Pomatoschistus minutus) that differ dramatically with respect to nest‐site density and the documented nature and intensity of sexual selection. At the Tvärminne site in the Baltic Sea, the microsatellite genotypes of 17 nest‐tending males and mean samples of more than 50 progeny per nest indicated that approximately 35% of the nests contained eggs that had been fertilized by sneaker males. Successful nest holders mated with an average of 3.0 females, and the distribution of mate numbers for these males did not differ significantly from the Poisson expectation. These genetically deduced mating‐system parameters in the Tvärminne population are remarkably similar to those in sand gobies at a distant site adjoining the North Sea. Thus, pronounced differences in the ecological setting and sexual selection regimes in these two populations have not translated into evident differences in cuckoldry rates or other monitored patterns of male mating success. In this case, the ecological setting appears not to be predictive of alternative male mating strategies, a finding of relevance to sexual selection theory.     

Distributional and demographic consequences of Pleistocene climate fluctuations for a marine demersal fish in the north-eastern Atlantic

Aim The Pleistocene glaciations were the most significant historical event during the evolutionary life span of most extant species. However, little is known about the consequences of these climate changes for the distribution and demography of marine animals of the north‐eastern Atlantic. The present study focuses on the phylogeographic and demographic patterns of the sand goby, Pomatoschistus minutus (Teleostei: Gobiidae), a small marine demersal fish. Location North‐eastern Atlantic, Mediterranean, Irish, North and Baltic seas. Methods Analysis was carried out by sequencing the mtDNA cytochrome b gene of sand gobies from 12 localities throughout the species’ range, and using this information in combination with published data of allozyme markers and mtDNA control region sequences. Several phylogenetic methods and a network analysis were used to explore the phylogeographic pattern. The historical demography of P. minutus was studied through a mismatch analysis and a Bayesian skyline plot. Results Reciprocal monophyly was found between a Mediterranean Sea (MS) clade and an Atlantic Ocean (AO) clade, both with a Middle Pleistocene origin. The AO Clade contains two evolutionary significant units (ESUs): the Iberian Peninsula (IB) Group and the North Atlantic (NA) Group. These two groups diverged during Middle Pleistocene glacial cycles. For the NA Group there is evidence for geographic sorting of the ancestral haplotypes with recent radiations in the Baltic Sea, Irish Sea, North Sea and Bay of Biscay. The demographic histories of the Mediterranean Clade and the two Atlantic ESUs were influenced mainly by expansions dated as occurring during the Middle Pleistocene glaciations and post‐Eem, respectively. Main conclusions The pre‐LGM (Last Glacial Maximum) subdivision signals were not erased for P. minutus during the LGM. Middle Pleistocene glaciations yielded isolated and differently evolving sets of populations. In contrast to the case for most other taxa, only the northern Atlantic group contributed to the post‐glacial recolonization. The historical demography of Mediterranean sand gobies was influenced mainly by Middle Pleistocene glaciations, in contrast to that of the Atlantic populations, which was shaped by Late Pleistocene expansions.     

To see in different seas: spatial variation in the rhodopsin gene of the sand goby (Pomatoschistus minutus)

Aquatic organisms living in a range of photic environments require specific mechanisms to tune their visual pigments. Maximum absorbance (λ_max) of retinal rods in populations of the marine demersal sand goby, ( Pomatoschistus minutus ; Gobiidae, Teleostei) correlates with the local optic environment. It has been shown that this is not regulated through a physiological response by exchanging the rhodopsin chromophore. To test for evolutionary adaptation, the sequence of the rhodopsin ( RH1 ) gene was analysed in 165 Pomatoschistus minutus individuals from seven populations across its distribution range. Analysis showed a high level of intraspecific polymorphism at the RH1 gene, including nonsynonymous mutations on amino acids, known as spectral tuning sites. Population differentiation at these sites was in agreement with the observed differentiation in λ_max values. Analyses of d _N/ d _S substitution rate ratios and likelihood ratio tests under site-specific models detected a significant signal of positive Darwinian selection on the RH1 gene. A strong discrepancy in differentiation was noticed between RH1 gene variation and the presumably neutral microsatellites and mitochondrial data. Samples did not cluster according to geographical or historical proximity with regards to RH1 , but according to the general photic conditions of the habitat environment of the sand goby. This study highlights the usefulness of sensory genes, like rhodopsin, for studying the characteristics of local adaptation in marine nonmodel organisms.     

Effects of current and historic habitat fragmentation on the genetic structure of the sand goby Pomatoschistus minutus (Osteichthys,Gobiidae)

Habitat fragmentation is a major force that will influence the evolution of a species and its distribution range. Pomatoschistus minutus, the sand goby, has a North Atlantic–Mediterranean distribution and shows various level of habitat fragmentation along its geographic repartition. The use of mitochondrial sequences of the cytochrome b (cyt b) gene and two co‐dominant sets of nuclear markers (introns and microsatellites) allowed us to describe the relationships between P. minutus populations belonging to several different geographical regions of Europe and to assess the structure of populations inhabiting the Golfe du Lion, along the French Mediterranean coast. The present study confirms that the taxon located in the Adriatic Sea (Venice) should be considered as a distinct species, separated approximately 1.75 Mya. The comparison of P. minutus between the Atlantic and western Mediterranean coasts using polymorphic co‐dominant markers revealed that they belong to two demographically independent units, and thus could be considered as well as distinct species, more recently separated (0.3 Mya). The Pleistocene glaciations seem therefore to have played an important role in the diversification of this complex. Finally, at a regional scale in the Golfe du Lion, P. minutus appears to form a single huge homogeneous population. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 175–198.     

Population genomic evidence for adaptive differentiation in the Baltic Sea herring

Detecting and estimating the degree of genetic differentiation among populations of highly mobile marine fish having pelagic larval stages is challenging because their effective population sizes can be large, and thus, little genetic drift and differentiation is expected in neutral genomic sites. However, genomic sites subject to directional selection stemming from variation in local environmental conditions can still show substantial genetic differentiation, yet these signatures can be hard to detect with low‐throughput approaches. Using a pooled RAD‐seq approach, we investigated genomewide patterns of genetic variability and differentiation within and among 20 populations of Atlantic herring in the Baltic Sea (and adjacent Atlantic sites), where previous low‐throughput studies and/or studies based on few populations have found limited evidence for genetic differentiation. Stringent quality control was applied in the filtering of 1 791 254 SNPs, resulting in a final data set of 68 182 polymorphic loci. Clear differentiation was identified between Atlantic and Baltic populations in many genomic sites, while differentiation within the Baltic Sea area was weaker and geographically less structured. However, outlier analyses – whether including all populations or only those within the Baltic Sea – uncovered hundreds of directionally selected loci in which variability was associated with either salinity, temperature or both. Hence, our results support the view that although the degree of genetic differentiation among Baltic Sea herring populations is low, there are many genomic regions showing elevated divergence, apparently as a response to temperature‐ and salinity‐related natural selection. As such, the results add to the increasing evidence of local adaptation in highly mobile marine organisms, and those in the young Baltic Sea in particular.     

Rhodopsin population genetics and local adaptation: variable dim-light vision in sand gobies is illuminated

The visual pigments of fish are thought to be adapted to the variable spectral qualities of aquatic light environments. Most research on the role of natural selection on the evolution of rhodopsins and dim-light vision in fish has focused on variation among species and higher taxa. In this issue, Larmuseau et al. reveal substantial intraspecific sequence variation in RH1 (the rhodopsin gene) in sand gobies ( Pomatoschistus minutus ). Using population genetics and molecular evolution approaches, they detect positive selection on RH1 and find evidence for adaptation to local light conditions.     

The importance of gobies (Gobiidae,Teleostei) as hosts and transmitters of parasites in the SW Baltic

The parasite fauna of five goby species (Gobiidae, Teleostei) was investigated in the Baltic Sea during the period 1987 to 1990. 13 parasite species were found in samples from the Lübeck Bight:Bothriocephalus scorpii, Schistocephalus sp. (Cestoda);Cryptocotyle concavum, Cryptocotyle lingua, Podocotyle atomon, Derogenes varicus (Digenea);Hysterothylacium sp. (cf.auctum),Contracaecum sp.,Anisakis simplex (Nematoda);Corynosoma sp.,Echinorhynchus gadi, Neoechinorhynchus rutili, Pomphorhynchus laevis (Acanthocephala). The number of parasite species were: 10 in the sand gobyPomatoschistus minutus, 8 in the black gobyGobius niger, 7 in the two-spotted gobyGobiusculus flavescens, 6 in the common gobyPomatoschistus microps, and 5 in the painted gobyPomatoschistus pictus. Neoechinorhynchus rutili occurred only inP. minutus, andCorynosoma sp. only inG. niger. The extent to which the gobies were parasitized clearly depended on the respective ways of life and, moreover, on the kind of prey ingested by the hosts. Additionally, the age of the hosts might be important. The highest rate of parasitism, more than 60%, was reached byHysterothylacium sp. inG. niger and byCryptocotyle concavum inP. microps. Infestation incidence lay mostly below 40% which means a satellite species status (Holmes, 1991). The number of parasite species was highest in summer; the highest intensities of single parasites occurred in spring (Podocotyle atomon) or autumn (Crytocotyle concavum).Bothriocephalus scorpii, Hysterothylacium sp. andPodocotyle infested their juvenile hosts very early, but onlyHysterothylacium was accumulated byG. niger during its whole life span, whereasBothriocephalus persisted also in older gobies in low intensities. The cercariae ofCryptocotyle spp. penetrate actively into their hosts; all the other parasites named were transmitted in larval form by prey organisms which consisted mainly of planktonic and benthic crustaceans. The gobies were final hosts for only 5 parasites; but two species may be transmitted to larger fish, and 6 species to sea birds or mammals. The parasite community of the five gobies may possibly be taken to characterize the ecological quality of the environment of the Lübeck Bight.     

Environmental factors influencing the gobiid assemblage of a Mediterranean Lagoon: Empirical evidence from a long-term study

A severe freshwater inflow during our long-term ichthyological study of the brackish Vaccarès lagoon (1993–1998) helped us to assess the impact of sudden environmental changes on the specific biomass composition of the gobiid population and the catches per unit effort of the black goby Gobius niger, the common goby Pomatoschistus microps and the sand goby P. minutus. In 1993, the composition of the Gobiid fish assemblage of the Vaccarès lagoon was dominated by the black goby (63%) and finally evolved to an assemblage dominated by the common goby (80%). The black goby disappeared from the Vaccarès lagoon 2 years after the inflow, whereas catches of the common goby increased significantly after the environmental changes and reached maximum values in 1998. Catches of sand goby did not seem to be affected by environmental changes and depended on the communication between sea and lagoon. This study showed that evolution of an ecosystem after environmental changes is linked to the reaction that species developed to face perturbations.     

Mitochondrial DNA phylogeography reveals the existence of an Evolutionarily Significant Unit of the sand goby Pomatoschistus minutus in the Adriatic (Eastern Mediterranean)

The sand goby Pomatoschistus minutus is a major component of marine shelf and estuarine food webs and an important study organism in behavioural research. Yet, despite the sand goby’s significance, its past and present patterns of migration and gene flow are poorly understood. Here we use the mtDNA control region and parts of the flanking tRNA genes of 63 fish from six localities in the Adriatic (Eastern Mediterranean), Western Mediterranean, Atlantic, and North Sea to investigate the phylogeography of this gobiid. Phylogenetic analyses and population genetics statistics reveal the existence of an Evolutionarily Significant Unit, sensu Moritz (1994), in the Adriatic and another in the Western Mediterranean, Atlantic, and North Sea. A possible biogeographical scenario for the separation of the ancestral population is that sand gobies in the Adriatic and Western Mediterranean split between 10,000 and 5000 years ago when due to the rise in sea temperature they migrated northwards and were bisected by the Italian peninsula. A testable prediction of this scenario is that sand gobies from the Western Mediterranean, Adriatic, and Aegean form three reciprocally monophyletic groups which are the descendants of a three-way diversification event.     

A new species of Pomatoschistus (Teleostei,Gobiidae): the Mediterranean's smallest marine fish

The new sand goby species Pomatoschistus nanus (Teleostei: Gobiidae) is described from the northern coast of the Levantine Sea (eastern Mediterranean Sea) based on both morphological and DNA barcoding data. The new species is the smallest fish in the Mediterranean Sea and may be distinguished from congeners by the following features: predorsal area, first dorsal‐fin base and breast naked; δ‐pore missing; anterior point of the suborbital row b not reaching level of posterior point of suborbital row d; slightly emarginated caudal fin and nape coloration pattern. DNA barcode data clearly discriminate Pomatoschistus spp. in the neighbour‐joining tree with an average of 17·7% interspecific K2P distance. The most closely related taxon to P. nanus sp. nov. is Pomatoschistus bathi and the most distantly related is Pomatoschistus tortonesei with 11·9 and 21·9% K2P distances respectively. Morphometric and genetic data are also provided for Pomatoschistus bathi.     

Phylogeographic evidence for the postglacial colonization of the North and Baltic Sea coasts from inland glacial refugia by Triglochin maritima L.

We investigated the geographical distribution of genetic variation in 67 individuals of Triglochin maritima from 38 localities across Europe using AFLP markers. Analysis of genetic variation resulted in the recognition of two major genetic groups. Apart from few geographical outliers, these are distributed (1) along the Atlantic coasts of Portugal, Spain and France and (2) in the North Sea area, the Baltic Sea area, at central European inland localities, the northern Adriatic Sea coast and the Mediterranean coast of southwest France. Considering possible range shifts of T. maritima in reaction to Quaternary climatic changes as deduced from the present-day northern temperature limit of the species, Quaternary changes of coastline in the North Sea area and the very recent origin of the Baltic Sea, we conclude that the coastal populations of T. maritima in the North Sea and Baltic Sea areas originated from inland populations.     

Genetic differentiation of southeast Baltic populations of sea trout inferred from single nucleotide polymorphisms

Sea trout (Salmo trutta m. trutta) is a migratory form of brown trout common in the Baltic Sea. Nine populations from the southeast Baltic (Poland; Lithuania; Denmark, Bornholm; Estonia and Russia) were genotyped using iPLEX Gold technology (Sequenom) with 62 informative SNPs. A diagnostic panel of 23 SNPs was applied to estimate genetic differentiation and assess the population structure of Baltic sea trout. The highest level of pairwise F_ST differences was observed between the Russian (East Gulf of Finland) and Polish (Baltic main basin) populations. The lowest differences were between the two Polish and the Polish and Lithuanian populations. A genetic similarity was noted between the Estonian Riguldi River and Danish Bornholm populations, and this finding was supported by a Bayesian and factorial correspondence analysis. Diversity within populations was highest for populations from Estonia and lowest for the Lithuanian population. Genetic structure analysis indicated that individuals from the nine populations were clustered into four groups.     

Seasonal migrations of the common Goby,Pomatoschistusmicrops (Kroyer), in Morecambe Bay and elsewhere

Summary Seasonal changes in abundance, and also reproduction, of the gobiid Pomatoschistus microps in intertidal pools on mussel beds at Morecambe, Lancashire, were studied from 1956 to 1961. During winter the shore was largely vacated by this species which returned for breeding purposes in spring. Spawning took place in upper shore pools from April to August. After a planktonic life of between 6–9 weeks, young fishes were recruited to the demersal population usually from June to September. A correlation between seasonal migrations and sea temperature is postulated. Geographical variation in occurrence and extent of migration in P. microps and the related sublittoral P. minutus is considered in relation to minimum winter sea temperatures over the southern Boreal and Baltic sea areas. Offshore winter migration has been found to take place in areas where such temperatures normally fall below 5° C, but not where minimum sea temperature is above 7° C. The effect of the severe winter of 1962–63 on certain populations of P. microps is described.     

Prey selection of the shallow water fishPomatoschistus minutus (Gobiidae,Teleostei) in the SW Baltic

The aim of this investigation is to demonstrate the reasons of an opportunist feeder to select some components of the available food supply and to avoid others. Object of this test is the eurytopic and euryhaline sand goby,Pomatoschistus minutus (Pallas), from the Luebeck Bight. It inhabits both sand habitats as well as bottoms mixed with pebbles or continuous hard substrates. Therefore, it is often in close contact withMytilus-belts which present a very rich food supply of small crustaceans. The selectivity behaviour of sand gobies from a sand/clay ecotone was compared with that of populations from a stony pier and a sand bottom during the reproduction period. Regarding the numbers of prey organisms, crustaceans of the periphyton were generally preferred at the pier but avoided in the ecotone. The same is valid for prey organisms of the psammal which were preferred by gobies of the sand bottom but mostly avoided by populations of mixed bottoms. Analyses of size selections revealed that the preferred gammarids orJaera isopods were between 2 and 5 mm length. A balanced relation of goby biomass and utilizable food supply (predatory impact index) seems to effect positive selectivity of gammarids in theMytilus-belts or of harpacticoids in the sand bottom.     

Molecular signatures of lineage‐specific adaptive evolution in a unique sea basin: the example of an anadromous goby Leucopsarion petersii

Climate changes on various time scales often shape genetic novelty and adaptive variation in many biotas. We explored molecular signatures of directional selection in populations of the ice goby Leucopsarion petersii inhabiting a unique sea basin, the Sea of Japan, where a wide variety of environments existed in the Pleistocene in relation to shifts in sea level by repeated glaciations. This species consisted of two historically allopatric lineages, the Japan Sea (JS) and Pacific Ocean (PO) lineages, and these have lived under contrasting marine environments that are expected to have imposed different selection regimes caused by past climatic and current oceanographic factors. We applied a limited genome‐scan approach using seven candidate genes for phenotypic differences between two lineages in combination with 100 anonymous microsatellite loci. Neuropeptide Y (NPY) gene, which is an important regulator of food intake and potent orexigenic agent, and three anonymous microsatellites were identified as robust outliers, that is, candidate loci potentially under directional selection, by multiple divergence‐ and diversity‐based outlier tests in comparisons focused on multiple populations of the JS vs. PO lineages. For these outlier loci, populations of the JS lineage had putative signals of selective sweeps. Additionally, real‐time quantitative PCR analysis using fish reared in a common environment showed a higher expression level for NPY gene in the JS lineage. Thus, this study succeeded in identifying candidate genomic regions under selection across populations of the JS lineage and provided evidence for lineage‐specific adaptive evolution in this unique sea basin.