Larval dispersal dampens population fluctuation and shapes the interspecific spatial distribution patterns of rocky intertidal gastropods

Many marine benthic invertebrates pass through a planktonic larval stage whereas others spend their entire lifetimes in benthic habitats. Recent studies indicate that non‐planktonic species show relatively greater fine‐scale patchiness than do planktonic species, but the underlying mechanisms remain unknown. One hypothesis for such a difference is that larval dispersal enhances the connectivity of populations and buffers population fluctuations and reduces local extinction risk, consequently increasing patch occupancy rate and decreasing spatial patchiness. If this mechanism does indeed play a significant role, then the distribution of non‐planktonic species should be more aggregated – both temporally and spatially – than the distribution of species with a planktonic larval stage. To test this prediction, we compared 1) both the spatial and the temporal abundance–occupancy relationships and 2) both the spatial and the temporal mean–variance relationships of population size across species of rocky intertidal gastropods with differing dispersive traits from the Pacific coast of Japan. We found that, compared to planktonic species, non‐planktonic species exhibited 1) a smaller occupancy rate for any given level of mean population size and 2) greater variations in population size, both spatially and temporally. This suggests that the macroecological patterns observed in this study (i.e. the abundance–occupancy relationships and mean–variance relationships of population size across species) were shaped by the effect of larval dispersal dampening population fluctuation, which works over both space and time. While it has been widely assumed that larval dispersal enhances population fluctuations, larval dispersal may in fact enhance the connectively of populations and buffer population fluctuations and reduce local extinction risks.     

Increased activity and growth rate in the non‐dispersive aquatic larval stage of a damselfly at an expanding range edge

相似文献   

Highly Connected Populations and Temporal Stability in Allelic Frequencies of a Harvested Crab from the Southern Pacific Coast

For marine invertebrates with a benthic adult form and a planktonic larva phase, the connectivity among populations is mainly based on larval dispersal. While an extended larval phase will promote gene flow, other factors such as an intensive fishery and geographical barriers could lead to changes in genetic variability. In this study, the population genetic structure of the commercial crab Metacarcinus edwardsii was analyzed along 700 km of the Chilean coast. The analysis, based on eight microsatellite loci genotyped from megalopae and adult crabs, considered temporal and spatial patterns of genetic variation. The results showed no evidence of spatial patterns in genetic structure, suggesting high connectivity among the sampling sites. The temporal analysis showed no evidence of changes in allele frequencies and no evidence of a recent bottleneck. The lack of spatial structure and allele variation over time could be explained by the interaction of factors such as i) low reproductive variance due to the capability of females to store sperm in the seminal receptacle, which can be used for successive broods, ii) high larval dispersal and iii) high individual reproductive output. Using our data as priors, a genetic modelling approach coincided, predicting this temporal and spatial stability. The same analysis showed that a reduction in population size leads to the loss of genetic variability in populations, as well as of the genetic cohesiveness between populations, pointing out the importance management for species under exploitation, such as M. edwardsii.     

Karyotypic changes associated to the dispersive potential on Pomacentridae (Pisces, Perciformes)

When comparing karyotypic diversification between freshwater and marine fish, a notable increase in modifications associated to the former environment can be noticed in relation to the latter one. This fact is related to the great number of physical partitions (barriers) that exist in continental waters. Furthermore, in the marine environment, the barriers to the gene flow are complex and not always identifiable, especially when considering the participation of dynamic factors such as currents and winds associated to the dispersive potentialities of a living group. Within Perciformes fish, the Pomacentridae family stands out from the others for its intimate relation with the coral reefs, as well as for its diversity of forms and biological characteristics, providing an adequate model for studying the influence of the pelagic period of the larval stage upon the karyotypic evolution. In the present work, cytogenetic analyses were carried out on three Pomacentridae species, typical representatives of the coral reefs, Abudefduf saxatilis (2n=48, FN=52, 2 m+2sm+44a), Microspathodon chrysurus (2n=48, FN=64, 6 m+10st+32a) and Amphiprion frenatus (2n=48, FN=92, 14 m+22sm+8st+4a) that have different pelagic larval periods. The analyses between subfamilies showed a trend that the lower the dispersive potential, the greater the quantity of fixed pericentric inversions based on the basal karyotype of the Perciformes.     

How useful are the genetic markers in attempts to understand and manage marine biodiversity?

The genetics of marine populations is a subject that has made little progress compared with the effort spent on the terrestrial environment. This is so despite “applied” aspects such as stock management, marine aquaculture, creation of reserves, conservation of the coastal zones, taxonomy, and protection of species. The crowded and dispersive marine environment, with its steep physical gradients, favours the existence of a planktonic larval stage for most species. The attendant high fecundity has important consequences for selection differentials and dispersal and therefore for the evolution of genetic structures. These features must be taken into account in order to understand the origin and maintenance of marine biodiversity and, in some cases, to manage it.In this article, after a definition of genetic diversity among other aspects of biodiversity, special features of the marine environment and processes governing genetic diversity are given together with the molecular tools required to study it. Then, an overview of the interesting scientific questions in marine biodiversity research is given concerning:

•

the population structure as a function of dispersal systems and spatial constraints: gene flow and speciation in a dispersive environment,

•

the phylogeography and historical biogeography of marine ecosystems;

•

the functional and adaptive aspects of polymorphism: larval phase and genetic control of recruitment.

Some uses of genetic diversity for assessment, conservation and protection purposes are also detailed. Organismal (specific) diversity does not enter the scope of the article.     

Influence of Biological Factors on Connectivity Patterns for Concholepas concholepas (loco) in Chile

In marine benthic ecosystems, larval connectivity is a major process influencing the maintenance and distribution of invertebrate populations. Larval connectivity is a complex process to study as it is determined by several interacting factors. Here we use an individual-based, biophysical model, to disentangle the effects of such factors, namely larval vertical migration, larval growth, larval mortality, adults fecundity, and habitat availability, for the marine gastropod Concholepas concholepas (loco) in Chile. Lower transport success and higher dispersal distances are observed including larval vertical migration in the model. We find an overall decrease in larval transport success to settlement areas from northern to southern Chile. This spatial gradient results from the combination of current direction and intensity, seawater temperature, and available habitat. From our simulated connectivity patterns we then identify subpopulations of loco along the Chilean coast, which could serve as a basis for spatial management of this resource in the future.     

Larval spatial distributions and other early life-history characteristics predict genetic differentiation in eastern Pacific blennioid fishes

In marine organisms, a pelagic larval stage increases the opportunities for long-distance dispersal and is often associated with little genetic differentiation over large geographical distances. Here we test the hypothesis that early life-history characteristics, including larval spatial distributions, affect the rates of dispersal and, therefore, the levels of genetic partitioning among three Gulf of California reef fishes: Axoclinus nigricaudus, Malacoctenus hubbsi and Ophioblennius steindachneri. These three blennioid fishes have markedly different early life histories: A. nigricaudus has a short larval duration (18 days) and develops inshore, M. hubbsi has an intermediate larval duration (24 days) and most individuals develop inshore and O. steindachneri has a long larval life (50 days) and disperses offshore. Estimates of genetic partitioning from mtDNA control region sequences differed greatly between these species and were in the same rank order as predicted by their early life-history characteristics (A. nigricaudus N(ST)=0.536, M. hubbsi N(ST)=0.261 and O. steindachneri N(ST)=0.000). These results indicate that larval strategies may be good predictors of population genetic structure in some marine fishes.     

Concordant geographic and genetic structure revealed by genotyping‐by‐sequencing in a New Zealand marine isopod

Population genetic structure in the marine environment can be influenced by life‐history traits such as developmental mode (biphasic, with distinct adult and larval morphology, and direct development, in which larvae resemble adults) or habitat specificity, as well as geography and selection. Developmental mode is thought to significantly influence dispersal, with direct developers expected to have much lower dispersal potential. However, this prediction can be complicated by the presence of geophysical barriers to dispersal. In this study, we use a panel of 8,020 SNPs to investigate population structure and biogeography over multiple spatial scales for a direct‐developing species, the New Zealand endemic marine isopod Isocladus armatus. Because our sampling range is intersected by two well‐known biogeographic barriers (the East Cape and the Cook Strait), our study provides an opportunity to understand how such barriers influence dispersal in direct developers. On a small spatial scale (20 km), gene flow between locations is extremely high, suggestive of an island model of migration. However, over larger spatial scales (600 km), populations exhibit a clear pattern of isolation‐by‐distance. Our results indicate that I. armatus exhibits significant migration across the hypothesized barriers and suggest that large‐scale ocean currents associated with these locations do not present a barrier to dispersal. Interestingly, we find evidence of a north‐south population genetic break occurring between Māhia and Wellington. While no known geophysical barrier is apparent in this area, it coincides with the location of a proposed border between bioregions. Analysis of loci under selection revealed that both isolation‐by‐distance and adaption may be contributing to the degree of population structure we have observed here. We conclude that developmental life history largely predicts dispersal in the intertidal isopod I. armatus. However, localized biogeographic processes can disrupt this expectation, and this may explain the potential meta‐population detected in the Auckland region.     

Isolation by resistance across a complex coral reef seascape

A detailed understanding of the genetic structure of populations and an accurate interpretation of processes driving contemporary patterns of gene flow are fundamental to successful spatial conservation management. The field of seascape genetics seeks to incorporate environmental variables and processes into analyses of population genetic data to improve our understanding of forces driving genetic divergence in the marine environment. Information about barriers to gene flow (such as ocean currents) is used to define a resistance surface to predict the spatial genetic structure of populations and explain deviations from the widely applied isolation-by-distance model. The majority of seascape approaches to date have been applied to linear coastal systems or at large spatial scales (more than 250 km), with very few applied to complex systems at regional spatial scales (less than 100 km). Here, we apply a seascape genetics approach to a peripheral population of the broadcast-spawning coral Acropora spicifera across the Houtman Abrolhos Islands, a high-latitude complex coral reef system off the central coast of Western Australia. We coupled population genetic data from a panel of microsatellite DNA markers with a biophysical dispersal model to test whether oceanographic processes could explain patterns of genetic divergence. We identified significant variation in allele frequencies over distances of less than 10 km, with significant differentiation occurring between adjacent sites but not between the most geographically distant ones. Recruitment probabilities between sites based on simulated larval dispersal were projected into a measure of resistance to connectivity that was significantly correlated with patterns of genetic divergence, demonstrating that patterns of spatial genetic structure are a function of restrictions to gene flow imposed by oceanographic currents. This study advances our understanding of the role of larval dispersal on the fine-scale genetic structure of coral populations across a complex island system and applies a methodological framework that can be tailored to suit a variety of marine organisms with a range of life-history characteristics.     

Kin-Aggregations Explain Chaotic Genetic Patchiness,a Commonly Observed Genetic Pattern,in a Marine Fish

The phenomenon of chaotic genetic patchiness is a pattern commonly seen in marine organisms, particularly those with demersal adults and pelagic larvae. This pattern is usually associated with sweepstakes recruitment and variable reproductive success. Here we investigate the biological underpinnings of this pattern in a species of marine goby Coryphopterus personatus. We find that populations of this species show tell-tale signs of chaotic genetic patchiness including: small, but significant, differences in genetic structure over short distances; a non-equilibrium or “chaotic” pattern of differentiation among locations in space; and within locus, within population deviations from the expectations of Hardy-Weinberg equilibrium (HWE). We show that despite having a pelagic larval stage, and a wide distribution across Caribbean coral reefs, this species forms groups of highly related individuals at small spatial scales (<10 metres). These spatially clustered family groups cause the observed deviations from HWE and local population differentiation, a finding that is rarely demonstrated, but could be more common than previously thought.     

Ocean circulation model predicts high genetic structure observed in a long‐lived pelagic developer

Understanding the movement of genes and individuals across marine seascapes is a long‐standing challenge in marine ecology and can inform our understanding of local adaptation, the persistence and movement of populations, and the spatial scale of effective management. Patterns of gene flow in the ocean are often inferred based on population genetic analyses coupled with knowledge of species' dispersive life histories. However, genetic structure is the result of time‐integrated processes and may not capture present‐day connectivity between populations. Here, we use a high‐resolution oceanographic circulation model to predict larval dispersal along the complex coastline of western Canada that includes the transition between two well‐studied zoogeographic provinces. We simulate dispersal in a benthic sea star with a 6–10 week pelagic larval phase and test predictions of this model against previously observed genetic structure including a strong phylogeographic break within the zoogeographical transition zone. We also test predictions with new genetic sampling in a site within the phylogeographic break. We find that the coupled genetic and circulation model predicts the high degree of genetic structure observed in this species, despite its long pelagic duration. High genetic structure on this complex coastline can thus be explained through ocean circulation patterns, which tend to retain passive larvae within 20–50 km of their parents, suggesting a necessity for close‐knit design of Marine Protected Area networks.     

Connectivity and Dispersal Patterns of Protected Biogenic Reefs: Implications for the Conservation of Modiolus modiolus (L.) in the Irish Sea

Biogenic reefs created by Modiolus modiolus (Linnaeus, 1758) (horse mussel reefs) are marine habitats which support high levels of species biodiversity and provide valuable ecosystem services. Currently, M. modiolus reefs are listed as a threatened and/or declining species and habitat in all OSPAR regions and thus are highlighted as a conservation priority under the EU Marine Strategy Framework Directive (MSFD). Determining patterns of larval dispersal and genetic connectivity of remaining horse mussel populations can inform management efforts and is a critical component of effective marine spatial planning (MSP). Larval dispersal patterns and genetic structure were determined for several M. modiolus bed populations in the Irish Sea including those in Wales (North Pen Llŷn), Isle of Man (Point of Ayre) and Northern Ireland (Ards Peninsula and Strangford Lough). Simulations of larval dispersal suggested extant connectivity between populations within the Irish Sea. Results from the genetic analysis carried out using newly developed microsatellite DNA markers were consistent with those of the biophysical model. Results indicated moderately significant differentiation between the Northern Ireland populations and those in the Isle of Man and Wales. Simulations of larval dispersal over a 30 day pelagic larval duration (PLD) suggest that connectivity over a spatial scale of 150km is possible between some source and sink populations. However, it appears unlikely that larvae from Northern Ireland will connect directly with sites on the Llŷn or Isle of Man. It also appears unlikely that larvae from the Llŷn connect directly to any of the other sites. Taken together the data establishes a baseline for underpinning management and conservation of these important and threatened marine habitats in the southern part of the known range.     

Weak genetic structure indicates strong dispersal limits: a tale of two coral reef fish

The extent of dispersal by pelagic larvae in marine environments, including coral reefs, is central for understanding local population dynamics and designing sustainable marine reserves. We present here the first example of a clear stepping-stone genetic structure throughout the Caribbean basin for a common coral reef species, the French grunt (Haemulon flavolineatum). Analysis of microsatellite DNA markers indicated that French grunt population structure may be characterized by overlapping populations throughout the Caribbean, influenced by independent population dynamics but with no fixed geographical boundaries. In addition, different spatial genetic patterns were found in different oceanographic regions. A second species, the bluehead wrasse (Thalassoma bifasciatum), has a much longer pelagic larval duration than French grunts and showed no explicit spatial pattern of genetic variation. This finding is concordant with the hypothesis of a positive relationship between larval dispersal and duration in the plankton. While the magnitude of the genetic signal of population structure in French grunts was very low (F(ST) approximately 0.003), the pattern of isolation-by-distance throughout the Caribbean indicated considerable population structure with important ecological and conservation significance.     

Nonsignificant isolation by distance implies limited dispersal

Understanding the scale of dispersal is an important consideration in the conservation and management of many species. However, in species in which the high‐dispersal stage is characterized by tiny gametes or offspring, it may be difficult to estimate dispersal directly. This is the case for many marine species, whose pelagic larvae are dispersed by ocean currents by several days or weeks before beginning a benthic, more sedentary, adult stage. As consequence of the high‐dispersal larval stage, many marine species have low genetic structure on large spatial scales (Waples 1998 ; Hellberg 2007 ). Despite the high capacity for dispersal, some tagging studies have found that a surprising number of larvae recruit into the population they were released from (self‐recruitment). However, estimates of self‐recruitment are not informative about mean dispersal between subpopulations. To what extent are limited dispersal estimates from tagging studies compatible with high potential for dispersal and low genetic structure? In this issue, a study on five species of coral reef fish used isolation by distance (IBD) between individuals to estimate mean dispersal distances (Puebla et al. 2012 ). They found that mean dispersal was unexpectedly small (<50 km), given relatively low IBD slopes and long pelagic durations. This study demonstrates how low genetic structure is compatible with limited dispersal in marine species. A comprehensive understanding of dispersal in marine species will involve integrating methods that estimate dispersal over different spatial and temporal scales. Genomic data may increase power to resolve these issues but must be applied carefully to this question.     

Spatial and temporal patterns of larval dispersal in a coral‐reef fish metapopulation: evidence of variable reproductive success

Many marine organisms can be transported hundreds of kilometres during their pelagic larval stage, yet little is known about spatial and temporal patterns of larval dispersal. Although traditional population‐genetic tools can be applied to infer movement of larvae on an evolutionary timescale, large effective population sizes and high rates of gene flow present serious challenges to documenting dispersal patterns over shorter, ecologically relevant, timescales. Here, we address these challenges by combining direct parentage analysis and indirect genetic analyses over a 4‐year period to document spatial and temporal patterns of larval dispersal in a common coral‐reef fish: the bicolour damselfish (Stegastes partitus). At four island locations surrounding Exuma Sound, Bahamas, including a long‐established marine reserve, we collected 3278 individuals and genotyped them at 10 microsatellite loci. Using Bayesian parentage analysis, we identified eight parent‐offspring pairs, thereby directly documenting dispersal distances ranging from 0 km (i.e., self‐recruitment) to 129 km (i.e., larval connectivity). Despite documenting substantial dispersal and gene flow between islands, we observed more self‐recruitment events than expected if the larvae were drawn from a common, well‐mixed pool (i.e., a completely open population). Additionally, we detected both spatial and temporal variation in signatures of sweepstakes and Wahlund effects. The high variance in reproductive success (i.e., ‘sweepstakes’) we observed may be influenced by seasonal mesoscale gyres present in the Exuma Sound, which play a prominent role in shaping local oceanographic patterns. This study documents the complex nature of larval dispersal in a coral‐reef fish, and highlights the importance of sampling multiple cohorts and coupling both direct and indirect genetic methods in order disentangle patterns of dispersal, gene flow and variable reproductive success.     

Asymmetric oceanographic processes mediate connectivity and population genetic structure,as revealed by RADseq,in a highly dispersive marine invertebrate (Parastichopus californicus)

Marine populations are typically characterized by weak genetic differentiation due to the potential for long‐distance dispersal favouring high levels of gene flow. However, strong directional advection of water masses or retentive hydrodynamic forces can influence the degree of genetic exchange among marine populations. To determine the oceanographic drivers of genetic structure in a highly dispersive marine invertebrate, the giant California sea cucumber (Parastichopus californicus), we first tested for the presence of genetic discontinuities along the coast of North America in the northeastern Pacific Ocean. Then, we tested two hypotheses regarding spatial processes influencing population structure: (i) isolation by distance (IBD: genetic structure is explained by geographic distance) and (ii) isolation by resistance (IBR: genetic structure is driven by ocean circulation). Using RADseq, we genotyped 717 individuals from 24 sampling locations across 2,719 neutral SNPs to assess the degree of population differentiation and integrated estimates of genetic variation with inferred connectivity probabilities from a biophysical model of larval dispersal mediated by ocean currents. We identified two clusters separating north and south regions, as well as significant, albeit weak, substructure within regions (F_ST = 0.002, p = .001). After modelling the asymmetric nature of ocean currents, we demonstrated that local oceanography (IBR) was a better predictor of genetic variation (R² = .49) than geographic distance (IBD) (R² = .18), and directional processes played an important role in shaping fine‐scale structure. Our study contributes to the growing body of literature identifying significant population structure in marine systems and has important implications for the spatial management of P. californicus and other exploited marine species.     

A new type of loriciferan larva (Shira larva) from the deep sea of Shatsky Rise,Pacific Ocean

Loricifera is a phylum of minute animals that live exclusively in marine sediments. A total of 33 species have been described so far in this phylum; however, several more are already known from preliminary observations. Loriciferans are characterised by a complex life cycle, which involves a succession of several adult and larval stages. Here, we describe a new type of loriciferan larval stage: the Shira larva. The gross morphology of this larva is generally similar to that of the most prominent larval type of Loricifera, the so-called Higgins larva. However, the Shira larva possesses a number of unique features, namely (1) a single pair of anteroventral setae is present in the most anterior region of the abdomen, (2) the bases of the anteroventral setae are very large and swollen, (3) the thorax and abdomen are thinner than the introvert and (4) the abdominal region is divided into five sub-regions. Accordingly, we described the new species, Tenuiloricus shirayamai gen. nov. et sp. nov. (incertae sedis). The new findings are discussed from a comparative perspective with the Higgins larva as well as with the fossil of a putative loriciferan larval stage from the Middle Cambrian.     

Spatial and genetic investigation of aggregation in Ischnochiton (Polyplacophora; Neoloricata; Ischnochitonina; Ischnochitonidae; Ischnochitoninae) species with different larval development

Many species are aggregated at some spatial scale but for some species, due to habitat or behaviour, aggregation can be difficult to assess quantitatively. Here, aggregation of chiton species (Polyplacophora; Neoloricata; Ischnochitonina; Ischnochitonidae; Ischnochitoninae; Ischnochiton) living under boulders in intertidal boulder fields was investigated at several relatively small spatial scales. Closely related species were found to be aggregated at the level of individual boulders, but evidence for grouping at the larger scale of patches of boulders varied. When organisms are mobile, dispersal can have an important influence on spatial patterns. Some organisms, such as marine invertebrates, have a highly dispersive larval phase that can influence spatial patterns of adults, particularly where the adult is sessile or relatively sedentary. Aggregation was compared in two species to test whether different modes of larval development influence spatial pattern. There was some evidence that species with a planktonic larva were even more aggregated than expected, in contrast to predictions based on this mode of development. Both types of larval development (planktonic and non‐planktonic) produce larvae with short development times in these species, so one possible explanation for the grouping habit of these chitons is that they do not disperse, at all, from their natal boulder. The complexity of the boulder field habitat and the cryptic behaviour of these chitons may also contribute to a lack of dispersal. A simple application of a genetic method indicated, however, that philopatry at this scale is unlikely.     

Fine scale dispersal in Banggai Cardinalfish, Pterapogon kauderni, a coral reef species lacking a pelagic larval phase

Dispersal in marine species results from complex interactions between biotic and abiotic factors. Importantly, the pelagic larval phase of most marine species adds a significant degree of complexity. Therefore, a growing body of work is focusing on those rare species that lack a pelagic larval phase (usually brooding species). For such species, large-scale gene flow has been shown to be very low, thus following the expectation of a relationship between realized dispersal and pelagic larval duration. Yet, little is known about the dispersal of those species at very small geographic scales. In this study, we focused on the Banggai Cardinalfish, Pterapogon kauderni, a mouthbrooding species that lacks a pelagic larval phase. Based on previously identified microsatellites, we scored 12 populations around the southern island of Bangkulu, in the Banggai Archipelago, Indonesia. While only 60 km in perimeter, we found that this island harbors very distinct populations of P. kauderni. Indeed, assignment tests self-assigned 10 out of those 12 populations. These results mirror the very high level of self-assignment at the level of the entire archipelago, where, out of 13 populations, 70% of the individuals were reassigned to their source population. Therefore, our data show consistency between small and large-scale dispersal. In addition, in light of the recent expansion in the harvesting of this species for the pet trade, our data have important conservation implications.     

Seascape and life-history traits do not predict self-recruitment in a coral reef fish

The persistence and resilience of many coral reef species are dependent on rates of connectivity among sub-populations. However, despite increasing research efforts, the spatial scale of larval dispersal remains unpredictable for most marine metapopulations. Here, we assess patterns of larval dispersal in the angelfish Centropyge bicolor in Kimbe Bay, Papua New Guinea, using parentage and sibling reconstruction analyses based on 23 microsatellite DNA loci. We found that, contrary to previous findings in this system, self-recruitment (SR) was virtually absent at both the reef (0.4–0.5% at 0.15 km²) and the lagoon scale (0.6–0.8% at approx. 700 km²). While approximately 25% of the collected juveniles were identified as potential siblings, the majority of sibling pairs were sampled from separate reefs. Integrating our findings with earlier research from the same system suggests that geographical setting and life-history traits alone are not suitable predictors of SR and that high levels of localized recruitment are not universal in coral reef fishes.