Population structure and connectivity in the Mediterranean sponge Ircinia fasciculata are affected by mass mortalities and hybridization

Abstract

Recent episodes of mass mortalities in the Mediterranean Sea have been reported for the closely related marine sponges Ircinia fasciculata and Ircinia variabilis that live in sympatry. In this context, the assessment of the genetic diversity, bottlenecks and connectivity of these sponges has become urgent in order to evaluate the potential effects of mass mortalities on their latitudinal range. Our study aims to establish (1) the genetic structure, connectivity and signs of bottlenecks across the populations of I. fasciculata and (2) the hybridization levels between I. fasciculata and I. variabilis. To accomplish the first objective, 194 individuals of I. fasciculata from 12 locations across the Mediterranean were genotyped at 14 microsatellite loci. For the second objective, mitochondrial cytochrome c oxidase subunit I sequences of 16 individuals from both species were analyzed along with genotypes at 12 microsatellite loci of 40 individuals coexisting in 3 Mediterranean populations. We detected strong genetic structure along the Mediterranean for I. fasciculata, with high levels of inbreeding in all locations and bottleneck signs in most locations. Oceanographic barriers like the Almeria-Oran front, North-Balearic front and the Ligurian-Thyrrenian barrier seem to be impeding gene flow for I. fasciculata, adding population divergence to the pattern of isolation by distance derived from the low dispersal abilities of sponge larvae. Hybridization between both species occurred in some populations that might be increasing genetic diversity and somewhat palliating the genetic loss caused by population decimation in I. fasciculata.

Implications of population connectivity studies for the design of marine protected areas in the deep sea: An example of a demosponge from the Clarion‐Clipperton Zone

“…In P. craigi , the effect of null alleles should be disregarded since the four different areas still showed a significant departure from HWE (Table ), although some of the populations showed no departure from HWE when removing the loci possibly affected by the presence of null alleles (3Ple, 10Ple, 11Ple and 19Ple). High F IS values and departure from HWE in P. craigi are likely related to the biology of the species, as has already been claimed in other studies on shallow‐water sponges (Chaves‐Fonnegra et al., ; Riesgo et al., ). Very little is known about the reproduction of deep sea sponges in general (Witte, ), and nothing about the reproduction of P. craigi in particular, but we suggest that one of the main reasons behind the high levels of inbreeding and deficit of heterozygosity might be self‐recruitment.…”

“…This may be a result of limited dispersal of either gametes or larvae in P. craigi , supported by the observation that deep sea currents in this area are weak and dispersal by currents is expected to be small between successive generations. Self‐recruitment also been suggested for other marine sessile invertebrates with larvae with low‐dispersal abilities, including both shallow‐water (e.g., Chaves‐Fonnegra et al., ; Pérez‐Portela et al., ; Riesgo et al., ) and deep sea species (Le Goff‐Vitry, Pybus, & Rogers, ). Finally, the Wahlund effect caused by subpopulation structure should not be ruled out as a possible reason explaining low levels of heterozygosity, since it has already been documented for sponges (Chaves‐Fonnegra et al., ) and cnidarians (Ledoux et al., ).…”

“…As it has recently been discussed by Riesgo et al. () and other studies, reasons explaining the high levels of homozygosity in sponge populations may include a significant effect of null alleles, high levels of inbreeding, selection against heterozygotes, the Wahlund effect or a combination of these (Freeland, Kirk, & Petersen, ). In P. craigi , the effect of null alleles should be disregarded since the four different areas still showed a significant departure from HWE (Table ), although some of the populations showed no departure from HWE when removing the loci possibly affected by the presence of null alleles (3Ple, 10Ple, 11Ple and 19Ple).…”

“…Interestingly, no IBD was detected for a hadal amphipod species of the genus Paralicella occurring in the Pacific, with geological events and topographical barriers most likely responsible for the major isolation observed among their populations (Ritchie et al., ). In contrast, IBD has also commonly been reported in shallow‐water sponges especially in studies comprising large‐scale sampling sites (Duran et al., ; Guardiola et al., ; Wörheide, Epp, & Macis, ) or even at smaller scales after removing from the analysis populations occurring in areas separated by well‐known oceanographic barriers (Riesgo et al., ), and has commonly been explained by low‐dispersal abilities of sponges. There is also a wealth of examples in other shallow‐water organisms showing IBD between their populations, even when considering species with presumably high dispersal abilities (Launey, Ledu, Boudry, Bonhomme, & Naciri‐Graven, ; Maier, Tollrian, Rinkevich, & Nürnberger, ; Zulliger, Tanner, Ruch, & Ribi, ).…”

“…Stylissa carteri (Giles et al., ); 7. Ircinia fasciculata (Riesgo et al., ); 8. Plenaster craigi (this study); 9.…”