Genetic connectivity of Pelagia noctiluca populations reveal spatial and temporal reproductive subunits
Pelagia noctiluca is the one of the most venomous jellyfish in the Mediterranean Sea and its recurrent outbreaks, reported since the seventeenth century, earned this species a reputation as a plague, attracting special interest and concern since the late seventies. Aggregations of hundreds of thousands or millions of individuals are not rare for this species, whose population abundances show large fluctuations. Indeed, sudden demographical outbreaks lasting one or more years are normally followed by abrupt collapses, apparently without any symptom of distress. Previous population genetics and phylogeographic studies focusing on P. noctiluca at a large scale in the Mediterranean Sea and eastern Atlantic Ocean indicated that high levels of gene flow allows for a great connectivity across very large areas, maintaining a substantial panmixia.
A set of species-specific microsatellite markers was developed (for the first time in Scyphozoa).
In order to elucidate the P. noctiluca population genetics in a more itemized way, VECTORS research developed a set of species-specific microsatellite markers (for the first time in Scyphozoa) and used them to genotype a total of 488 P. noctiluca individuals from 10 geographic locations in the Mediterranean Sea and one site in the northeast Atlantic Ocean1. Moreover, the sampling was replicated in time for two populations in the southern Tyrrhenian Sea: for three consecutive years (2010-2011-2012) in one location (Ustica Island) and for two consecutive years (2011-2012) in another one (Strait of Messina). The samples of the geographically restricted area of southern Tyrrhenian Sea were first selected to investigate the processes governing the genetic behaviour of the single “bloom units”, namely the fluctuating agglomerates of jellyfish considered as separate populations. Pelagia noctiluca blooming in the southern Tyrrhenian Sea exhibited significant deviation from the Hardy-Weinberg equilibrium due to a large excess of homozygotes across 8 of 9 microsatellite loci, leading to high inbreeding coefficients (FIS). The results of sibship and parentage analyses supported the high inbreeding values by detecting intra-population relatedness higher than expected by chance (P<0.05) in at least three samples and siblings in at least 5 out 8 samples, 4 of which contained full-sib in addition to half-sib dyads. The genetic differentiation among populations was globally small (FST =0.01714; P<0.0001) but highlighted: a) a spatial genetic patchiness uncorrelated with distance between sampling locations, and b) a significant (P<0.0001) genetic heterogeneity between samples collected in the same locations in different years.
The great dispersal potential of P. noctiluca individuals guarantees high gene flows among the populations in a large geographic area.
These findings were concordant with those of the large spatial scale study, carried out to infer the population structure of P. noctiluca across the Mediterranean Sea and northeast Atlantic Ocean. In fact, almost all the populations of the study area exhibited high levels of inbreeding, as highlighted by substantial and positive FIS values. The spatial genetic structure analysis did not recognise any strong genetic structure in the whole study area, confirming that the great dispersal potential of P. noctiluca individuals guarantees high gene flows among the populations in a large geographic area. Nevertheless, a low (but statistically significant) and apparently unexplainable genetic differentiation (overall FST= 0.01149) was found between some populations in the study area.
Pelagia noctiluca in the Mediterranean Sea and Atlantic Ocean does not maintain a single perfectly homogenous population.
The patterns of genetic differentiation, such as those found in the small and large scale population genetics studies in P. noctiluca, are known as “chaotic genetic patchiness” or “fluctuating genetic mosaics”, commonly found in species characterised by high dispersal potential, as benthic marine invertebrates with a pelagic larval stage. Variability in reproductive success of the single individuals and genetic drift linked to high mortality rates in early life stages are usually considered the most important causes of these kinds of genetic patterns. In P. noctiluca, some specific features were identified as responsible for the genetic patchiness:
each mature female jellyfish spawns oocytes in a sticky mucus ribbon, holding eggs together for several minutes before its dissolution. This peculiarity may favour fertilization of the whole set of oocytes by sperms released by a single or a few male mates, producing a large amount of full sibs;
fusion of gametes produced by related individuals and the resultant formation of inbred offspring may be favoured by aggregative swimming behaviour of jellyfish. In fact, related individuals born from the same parental group at the same time have a reasonable probability of remaining together in the native bloom unit and hence also during subsequent spawning events, increasing the probability to produce inbred offspring (Fig. 1);
maintenance of kin-related jellyfish aggregation along marine currents may be influenced by small-scale hydrodynamic and oceanographic patterns conducive to limited individual mixing despite the high dispersal potential. Hydrogeographic features such as eddies, gyres or upwelling fronts could promote the aggregation of some groups of medusae in confined areas, preventing an extensive mixing with individuals belonging to other aggregations and allowing the fusion between gametes produced by related individuals (Fig. 2).
These physiological (a), behavioural (b) and environmental (c) factors might generate a strong variance in the reproductive success of P. noctiluca individuals. Indeed, if just a few males achieve the objective of reproduction, and the probability of union between gametes is not random (as indicated by the strong inbreeding), the generated recruit pools can have an unbalanced genetic composition with respect to the rest of the population<sup>2</sup>.
According to these results, P. noctiluca in the Mediterranean Sea and Atlantic Ocean does not maintain a single perfectly homogenous population (i.e. panmixia), even if the high gene flow avoids the establishment of strong genetic structures. Rather, the non-random mating among individuals and the influence of stochastic environmental factors shape the population genetics of this species generating a spatially and temporally fluctuating genetic patchiness.
This work was based on available samples deposited at the VECTORS repository DNA/tissue bank at the University of Salento (see Deliverable 3.2.2 for further information on the repository).
Relevance for Policy:
- Alien Invasive Species Directive
- Convention on Biological Diversity
- EU Biodiversity Strategy
- International Convention for the Control and Management of Ship's Ballast Water and Sediments