Spatial graphs highlight how multi-generational dispersal shapes landscape genetic patterns

Current approaches that compare spatial genetic structure of a given species and the dispersal of its mobile phase can detect a mismatch between both patterns mainly due to processes acting at different temporal scales. Genetic structure result from gene flow and other evolutionary and demographic processes over many generations, while dispersal predicted from the mobile phase often represents solely one generation on a single time-step. In this study, we present a spatial graph approach to landscape genetics that extends connectivity networks with a stepping-stone model to represent dispersal between suitable habitat patches over multiple generations. We illustrate the approach with the case of the striped red mullet Mullus surmuletus in the Mediterranean Sea. The genetic connectivity of M. surmuletus was not correlate with the estimated dispersal probability over one generation, but with the stepping-stone estimate of larval dispersal, revealing the temporal scale of connectivity across the Mediterranean Sea. Our results highlight the importance of considering multiple generations and different time scales when relating demographic and genetic connectivity. The spatial graph of genetic distances further untangles intra-population genetic structure revealing the Siculo-Tunisian Strait as an important corridor rather than a barrier for gene flow between the Western- and Eastern Mediterranean basins, and identifying Mediterranean islands as important stepping-stones for gene flow between continental populations. Our approach can be easily extended to other systems and environments.     

DISTRIBUTION and NUMBERS OF STRIPED DOLPHINS IN THE WESTERN MEDITERRANEAN SEA AFTER THE 1990 EPIZOOTIC OUTBREAK

A survey was conducted in the summer of 1991 in the western Mediterranean to map the distribution and to estimate the number of striped dolphins surviving the 1990 outbreak of the morbillivirus epizootic. The highest densities of striped dolphins were found in the Alboran Sea and the Ligurian Sea. Total numbers were estimated at 117,880 (SE: 38,962; 95% CI: 68,379–214,800). The mortality resulting from the epizootic is unknown but may have been severe because the mean size of dolphin schools observed during the epizootic outbreak was significantly smaller than that before the event. A return to larger school sizes after the 1990 outbreak is not evidence of a recovery but can be viewed as a regrouping of individuals into schools of a preferred size. Calves were observed in 24.6% of the schools. They were not seen in schools of ten or less but were present in about half the schools of 30 or more dolphins, a result which suggests segregation similar to that seen in populations of this species elsewhere in the world.     

Phenotypic Changes Across a Geographic Gradient: The Case of Three Sympatric Dolphin Species

Phenotypic changes in the mammalian mandible can occur at different spatial and temporal scales. We investigated mandibular size and shape variation in three extant closely related dolphins (Cetacea, Odontoceti): Tursiops truncatus, Stenella coeruleoalba and Delphinus delphis in order to test the hypothesis that similar phenotypic changes occur across the same geographical gradient. Our data included 219 specimens representative of the following geographic locations: the Mediterranean Sea, the eastern north Atlantic and the North Sea. Each mandibula was photographed laterally and spatial positioning of eight homologous 2D landmarks was recorded. After applying generalised Procrustes analysis (GPA), intraspecific variation was first investigated between sexes and among populations to allow further pooling of samples. Size and shape differences among populations and species were investigated through multivariate ordination techniques (PCA), Procrustes ANOVA and allometric analyses. In all three species, Mediterranean populations clearly differed in mandible shape from the extra-Mediterranean ones. Among the three, the direction of geographic phenotypic changes was significantly similar in the striped and common dolphin, while the bottlenose dolphin was the most divergent species, differing both in size and allometric trajectory. Shape variation of the two former species highlighted a morphological convergence in the Atlantic, and a phenotypic divergence in the Mediterranean. Shape differences among the three dolphin species were interpreted in the light of different prey preferences, feeding strategies and habitat partitioning to avoid direct competition.     

Social kin associations and genetic structuring of striped dolphin populations (Stenella coeruleoalba) in the Mediterranean Sea

We investigated hierarchical patterns of genetic subdivision, and assessed kinship within and between social groups of striped dolphins (Stenella coeruleoalba) in the Tyrrhenian Sea. A total of 165 samples were analysed at eight microsatellite DNA loci, including outgroup samples from the Adriatic, Scotland and Spain for population-level comparisons. We found population genetic structure within the Mediterranean basin, including small but significant differentiation between the Adriatic and Tyrrhenian Seas (FST=0.0047, P=0.008), and between putative 'inshore' and 'offshore' (FST=0.0217, P=0.005) populations in the Tyrrhenian Sea. Assessment of kinship within and among 12 association groups showed higher average kinship for females within than between groups, and smaller groups showed higher average kinship. Comparisons of relatedness for both sexes showed a significant difference between males and females, with females more likely to associate with adult kin. Together these data emphasize the importance of the social cohesion of kin in small groups to the structuring of striped dolphin populations in this environment.     

Fission‐fusion dynamics of Guiana dolphin (Sotalia guianensis) groups at Pipa Bay,Rio Grande do Norte,Brazil

Fission‐fusion dynamics seem to reflect individual decisions as well as temporal and spatial variations in the organization of groups of the same species. To understand the group dynamics of the Guiana dolphin, Sotalia guianensis, at Pipa Bay, Brazil, we investigated the three dimensions of a fission‐fusion social system: (1) variation in spatial cohesion, (2) variation in party size, and (3) variation in party composition. Sampling took place from December 2007 to February 2009 over 176 d and we analyzed the behavioral patterns of 658 groups. Within subgroups, animals remained cohesive, particularly in groups of adults and calves. Greater cohesion was also observed during resting and fission‐fusion rates were higher during milling and feeding. Groups composed of adults and juveniles showed a higher dynamics index (group size variation as a function of time) than groups composed only of adults and the fission‐fusion rate was higher during dry periods. Guiana dolphin groups frequently changed their group size and composition every 20 min on average. Taking these factors into consideration, we suggest that the Guiana dolphin demonstrates fission‐fusion dynamics, a pattern of behavior similar to what has been observed in other coastal odontocete species, such as Tursiops spp. and Lagenorhynchus obscurus.     

Genetic isolation of a now extinct population of bottlenose dolphins (Tursiops truncatus)

A number of dolphin species, though highly mobile, show genetic structure among parapatric and sometimes sympatric populations. However, little is known about the temporal patterns of population structure for these species. Here, we apply Bayesian inference and data from ancient DNA to assess the structure and dynamics of bottlenose dolphin (Tursiops truncatus) populations in the coastal waters of the UK. We show that regional population structure in UK waters is consistent with earlier studies suggesting local habitat dependence for this species in the Mediterranean Sea and North Atlantic. One genetically differentiated UK population went extinct at least 100 years ago and has not been replaced. The data indicate that this was a local extinction, and not a case of historical range shift or contraction. One possible interpretation is a declining metapopulation and conservation need for this species in the UK.     

Length–weight relationships for the family Triglidae in the Adriatic Sea,northeastern Mediterranean

Length–weight relationships were estimated for the first time for seven species of gurnards (Triglidae) based on data collected over the past 27 years in the Adriatic Sea (northeast Mediterranean). Results show significantly different relationships between juveniles and adults (females and males combined) for Aspitrigla cuculus, Eutrigla gurnardus, Chelidonichthys lucerna and Lepidotrigla cavillone. Isometric growth of juveniles is indicated for four species, allometric growth of adults for all species.     

Comparative study on the fatty acid composition of two marine vertebrates: striped dolphins and loggerhead turtles

The fatty acid composition of total lipids extracted from seven different tissues (fat, liver, cerebrum, cerebellum, lung, kidney and muscle) of 10 striped dolphins (Stenella coeruleoalba) (weight 75.7±16.2 kg) found dead or moribund during a morbillivirus epizootic, and from two tissues (fat and liver) of 54 loggerhead turtles (Caretta caretta) (18.5±10.5 kg) seized dead after illegal capture, both from the Mediterranean Sea, have been determined by high resolution chromatography techniques. When comparing both species, fatty acid composition is surprisingly similar, with a predominance of the monoenoic followed by the saturated group of fatty acids, and a very close ratio of polyunsaturates n-3/n-6. The relatively high arachidonic acid content in the liver of the two marine species is remarkable. The similar diet can play an important role in these findings, but it is suggested that probably metabolic pathways and essential fatty acid requirements between both marine vertebrates are similar, more than is expected from their earlier filogenetic evolutionary divergence.     

Unexpected collective larval dispersal but little support for sweepstakes reproductive success in the highly dispersive brooding mollusc Crepidula fornicata

In many marine invertebrates, long‐distance dispersal is achieved during an extended pelagic larval phase. Although such dispersal should result in high gene flow over broad spatial scales, fine‐scale genetic structure has often been reported, a pattern attributed to interfamilial variance in reproductive success and limited homogenization during dispersal. To examine this hypothesis, the genetic diversity of dispersing larvae must be compared with the postdispersal stages, that is benthic recruits and adults. Such data remain, however, scarce due to the difficulty to sample and analyse larvae of minute size. Here, we carried out such an investigation using the marine gastropod Crepidula fornicata. Field sampling of three to four larval pools was conducted over the reproductive season and repeated over 3 years. The genetic composition of larval pools, obtained with 16 microsatellite loci, was compared with that of recruits and adults sampled from the same site and years. In contrast to samples of juveniles and adults, large genetic temporal variations between larval pools produced at different times of the same reproductive season were observed. In addition, full‐ and half‐sibs were detected in early larvae and postdispersal juveniles, pointing to correlated dispersal paths between several pairs of individuals. Inbred larvae were also identified. Such collective larval dispersal was unexpected given the long larval duration of the study species. Our results suggest that each larval pool is produced by a small effective number of reproducers but that, over a reproductive season, the whole larval pool is produced by large numbers of reproducers across space and time.     

MITOCHONDRIAL DNA VARIABILITY OF STRIPED DOLPHINS (STENELLA COERULEOALBA) IN THE SPANISH MEDITERRANEAN WATERS

Frozen muscle samples from 44 striped dolphins stranded on the Spanish Mediterranean coasts from 1990 to 1993 have been studied by means of mitochondrial DNA (mtDNA) restriction site analysis. Thirty-five of these dolphins were affected by a die-off occurring during this time in the western Mediterranean Sea. The mtDNA from each dolphin was digested with 15 restriction endonucleases that recognized 61 different restriction sites. The specific location of these sites on the mitochondrial gene map allowed us to determine the distribution of variability along this molecule. From the restriction analysis, a total of 15 different composite patterns or haplotypes was obtained and their phylogenetic relationships established both by cladistic and phenetic methods.
Estimates of sequence divergence among the 15 haplotypes ranged from 0.148% to 0.919%. Haplotype diversity (average heterozygosity) obtained was 0.789, a high value compared to other available data on cetaceans, especially considering that only a small area of the distribution of the species has been sampled. Neither population subdivision nor any evidence of correlation between haplotype frequencies and temporal or geographic distribution of dolphins has been detected.     

Detecting immigrants in a highly genetically homogeneous spiny lobster population (Palinurus elephas) in the northwest Mediterranean Sea

We investigated the genetic structure of early benthic juveniles of the spiny lobster Palinurus elephas in the northwest Mediterranean Sea by means of ten polymorphic microsatellite markers. Non‐metric Multidimensional Scaling coupled with assignment tests were used as a new approach to further delimit a reference population inside a genetically homogeneous pool of individuals and test for the presence of long distance immigrants. From this approach, we found that most early benthic juveniles collected while settling in the northwest Mediterranean Sea originated from a common larval pool. However, 4.2% of the individuals were classified as immigrants from other genetically differentiated populations, with more immigrants in the south than in the north of the sampled basin. Given currents in the northwest Mediterranean Sea and the long pelagic larval phase of P. elephas that lasts several months, this result suggest a restricted homogenized zone in the studied basin with some individuals probably coming from more differentiated populations through the Almeria‐Oran Front or the Strait of Sicily.     

Spatial and temporal variability among marine Bacteroidetes populations in the NW Mediterranean Sea

The abundance and structure of Bacteroidetes populations at diverse temporal and spatial scales were investigated in the Northwestern Mediterranean Sea. At a temporal scale, their relative abundance exhibited a marked seasonality, since it was higher in spring and decreased in winter. Similarly, Bacteroidetes community structure encompassed three main groups (winter, spring and summer-fall), which mimicked global bacterioplankton seasonality. At the spatial scale, relative abundances were similar in all surface samples along an inshore–offshore transect, but they decreased with depth. Analysis of the community structure identified four markedly different groups mostly related to different depths. Interestingly, seasonal changes in abundance and community structure were not synchronized. Furthermore, richness was higher when Bacteroidetes were less abundant. The variability of Bacteroidetes contributions to community structure in the temporal and spatial scales was correlated with different environmental factors: day length was the most important factor at the temporal scale, and salinity at the spatial scale. The community composition in terms of phylotypes changed significantly over time and along the depth gradients, but season or depth-specific phylogenetic clusters were not identified. Delineation of coherent Bacteroidetes sub-clusters should help to uncover higher resolution patterns within Bacteroidetes, and explore associations with environmental and biological variables.     

Overfishing of small pelagic fishes increases trophic overlap between immature and mature striped dolphins in the Mediterranean Sea

The interactions among diet, ecology, physiology, and biochemistry affect N and C stable isotope signatures in animal tissues. Here, we examined if ecological segregation among animals in relation to sex and age existed by analyzing the signatures of δ(15)N and δ(13)C in the muscle of Western Mediterranean striped dolphins. Moreover, we used a Bayesian mixing model to study diet composition and investigated potential dietary changes over the last two decades in this population. For this, we compared isotope signatures in samples of stranded dolphins obtained during two epizootic events occurring in 1990 and 2007-2008. Mean δ(13)C values for females and males were not significantly different, but age-related variation indicated δ(13)C enrichment in both sexes, suggesting that females and males most likely fed in the same general areas, increasing their consumption of benthic prey with age. Enrichment of δ(15)N was only observed in females, suggesting a preference for larger or higher trophic level prey than males, which could reflect different nutritional requirements. δ(13)C values showed no temporal variation, although the mean δ(15)N signature decreased from 1990 to 2007-2008, which could indicate a dietary shift in the striped dolphin over the last two decades. The results of SIAR indicated that in 1990, hake and sardine together contributed to 60% on the diet of immature striped dolphins, and close to 90% for mature striped dolphins. Conversely, the diet of both groups in 2007-2008 was more diverse, as hake and sardine contributed to less than 40% of the entire diet. These results suggest a dietary change that was possibly related to changes in food availability, which is consistent with the depletion of sardine stocks by fishing.     

Why Do Dolphins Form Mixed‐Species Associations in the Azores?

Mixed‐species associations are temporary associations between individuals of different species that are often observed in birds, primates and cetaceans. They have been interpreted as a strategy to reduce predation risk, enhance foraging success and/or provide a social advantage. In the archipelago of the Azores, four species of dolphins are commonly involved in mixed‐species associations: the common dolphin, Delphinus delphis, the bottlenose dolphin, Tursiops truncatus, the striped dolphin, Stenella coeruleoalba, and the spotted dolphin, Stenella frontalis. In order to understand the reasons why dolphins associate, we analysed field data collected since 1999 by research scientists and trained observers placed onboard fishing vessels. In total, 113 mixed‐species groups were observed out of 5720 sightings. The temporal distribution, habitat (water depth, distance to the coast), behaviour (i.e. feeding, travelling, socializing), size and composition of mixed‐species groups were compared with those of single‐species groups. Results did not support the predation avoidance hypothesis and gave little support to the social advantage hypothesis. The foraging advantage hypothesis was the most convincing. However, the benefits of mixed‐species associations appeared to depend on the species. Associations were likely to be opportunistic in the larger bottlenose dolphin, while there seemed to be some evolutionary constraints favouring associations in the rarer striped dolphin. Comparison with previous studies suggests that the formation of mixed‐species groups depends on several environmental factors, and therefore may constitute an adaptive response.     

Analysis of genetic structure of the red shrimp <Emphasis Type="Italic">Aristeus antennatus</Emphasis> from the Western Mediterranean employing two mitochondrial regions

In this paper we addressed the phylogeographical genetic structure of the economically important red shrimp, Aristeus antennatus (Crustacea, Aristeidae) in the Western Mediterranean. Partial mitochondrial regions of the cytochrome c oxidase subunit I (514 bp) and ribosomal 16S subunit (547 bp) were sequenced in 137 individuals collected at three localities: Catalan Sea, Ligurian Sea and the southern Tyrrhenian Sea. Values of haplotypic diversity were h = 0.552–0.724, whereas those for nucleotide diversity were π = 0.0012–0.0026. Among-sample genetic diversity was not significant and no geographical patterns in the distribution of haplotypes were apparent. Results of the present study are consistent with a past population expansion that occurred <2,000 years ago. Despite the current fishing pressure, genetic variability appears to be sufficiently high to keep A. antennatus populations stable over time. Dispersal-related life history traits may account for the shallow genetic structure. Our results are not in contrast with the hypothesis of sustainability of Western Mediterranean red shrimp fisheries predicted on the basis of previously obtained biological results.     

Variation in spatial distribution of juvenile loggerhead turtles in the eastern Atlantic and western Mediterranean Sea

Loggerhead sea turtles (Caretta caretta) originating from the Western Atlantic carry out one of the largest marine migrations, reaching the eastern Atlantic and Mediterranean Sea. It has been proposed that this transatlantic journey is simply a consequence of drifting, with the lack of a target destination and a passive dispersal with oceanic currents. This predicts that the size of the source populations and geographic distance to the feeding grounds should play important roles in defining stock composition in the eastern Atlantic and Mediterranean Sea. Under this scenario, near pelagic stocks would have no genetic structure, and would be composed of similar cohorts from regional rookeries. To address this question, we sampled individuals from one important eastern Atlantic feeding ground, the Canary Islands, and sequenced a fragment of the mitochondrial DNA control region. We compared the composition of this feeding stock with published data of other proximal areas: Madeira, Azores and Andalusia. “Rookery-centric” mixed stock analysis showed that the distribution of loggerhead sea turtles along the eastern Atlantic feeding grounds was in latitudinal accordance to their natal origin: loggerhead turtles from Florida were significantly more abundant in Azores (30%) than in Canary Islands (13%), while those from Mexico had a poor representation in Azores (13%) but were more prevalent in Canary Islands (34%). Also, genetic stability in temporal and size analyses of the Canary Island aggregation was found, showing a long period of residency. These results indicate a non-random distribution of loggerhead juveniles in oceanic foraging grounds. We discuss possible explanations to this latitudinal variation.     

Temporal and spatial variation of dominant pelagic Copepoda (Crustacea) in the Weddell Sea (Southern Ocean) 1929 to 1993

The abundances of four dominant Antarctic copepod species, Metridia gerlachei, Rhincalanus gigas, Calanoides acutus and Calanus propinquus, were examined in the Southern Ocean in a combination of a literature review, analysis of museum samples and field sampling. The data were analysed for spatial and temporal variations. The data included in the analysis were from the Weddell Sea area in the summertime at periods 1929–1939 and 1989–1993. The results are discussed in the light of environmental changes and their hypothesised and observed consequences in the Southern Ocean: global temperature change, ozone deficiency and cascading trophic interactions. Combining all these hypothetical effects our null hypothesis was that there were no consistent long-term changes in the abundance of dominant pelagic Copepoda. The null hypothesis was rejected, since several taxons did show statistically significant long-term changes in abundance. The changes were not uniform however. The numbers of adults and juveniles of Calanus propinquus increased significantly between the periods studied. Adult stages of Calanoides acutus were the only taxon decreasing in abundance, in concert with the cascading trophic interactions theory. Latitudinally, only Metridia gerlachei showed a significant increase from north to south. Longitudinally, the abundances of Calanus propinquus juveniles and both adults and juveniles of Rhincalanus gigas increased from west to east. There were no significant variations between day and night samples. Interannual changes were statistically significant in juvenile stages of all the species and in adults of Calanus propinquus. We conclude that no uniform and consistent abundance changes could be observed in the pelagic Copepoda of the Weddell Sea that could be connected to major environmental changes, expected to affect the whole planktonic ecosystem of the Southern Ocean. Significant changes in some of the species studied show that the pelagic ecosystem is not in a steady state, but in addition to interannual changes, there are also major fluctuations extending over decades. Received: 5 December 1996 / Accepted: 24 March 1997     

Discrepancies in phylogeographical patterns of two European anglerfishes (Lophius budegassa and Lophius piscatorius)

In order to investigate the relative importance of historical processes and life-history traits in shaping the present-day genetic structure of European anglerfishes, 382 Lophius piscatorius and 134 Lophius budegassa were sequenced on the 5' end of the mitochondrial control region. Both species showed a limited genetic structure and some evidence of a demographic expansion that probably occurred not at the end of the Last Glacial Maximum, but earlier in the Pleistocene. The main discrepancy between the two anglerfishes concerned the genetic structure between Atlantic and Mediterranean populations, with weak but significant differentiation observed only in L. budegassa. This genetic structure was congruent with the existence of a phylogeographical break previously reported in several marine species across the Almeria-Oran front. The contrast observed between both anglerfishes was supposed to be induced by a possible more ancient (re)colonisation of the Mediterranean Sea by L. budegassa. Finally, the limited genetic structure and lack of isolation by distance observed in both species suggested high larval dispersal capacities that probably overwhelm the influence of the bathymetric distribution range on migrations of adults and juveniles.     

Changes in epizoic crustacean infestations during cetacean die-offs: the mass mortality of Mediterranean striped dolphins Stenella coeruleoalba revisited

In the summer and autumn of 1990, a cetacean morbillivirus caused a massive epizootic mortality of striped dolphins Stenella coeruleoalba in the western Mediterranean. Previous circumstantial evidence suggested that the disease could also have increased host susceptibility to infestations with epizoic crustaceans. In this study we provide strong evidence supporting this hypothesis. We examined striped dolphins stranded along the Mediterranean central coast of Spain from 1981 to 2004 (n = 136), and recorded data on prevalence, intensity of infestation, size and reproductive status of 2 sessile crustacean species specific to cetaceans, the phoront cirriped Xenobalanus globicipitis and the mesoparasitic copepod Pennella balaenopterae. Compared with the pre-epizootic (n = 12) and post-epizootic (n = 62) dolphin samples, the following changes were noted in the dolphins stranded during the epizootic (n = 62): (1) the prevalence of both X. globicipitis and P. balaenopterae increased; (2) the intensity of X. globicipitis and P. balaenopterae infestations did not increase; indeed, it was even slightly lower than in the other periods, as was their degree of aggregation; (3) individuals of both species were smaller, and a higher proportion were non-gravid; (4) the 2 species tended to co-occur in the same dolphins, but their numbers did not co-vary. These patterns strongly suggest that, during the epizootic, there was a short-term increase in the probability of infestation of these 2 species because of the sudden rise in the population of susceptible hosts; the growth of the new recruits was limited by the early death of dolphins. The high susceptibility was likely related to the immunosuppressive effects of viral infection and the abnormally heavy loads of polychlorinated biphenyls found in sick dolphins; the level of inbreeding was also higher in dolphins from the 'epizootic' sample. Epizoic crustaceans could be suitable indicators of health in cetacean populations.