Population co-divergence in common cuttlefish (Sepia officinalis) and its dicyemid parasite in the Mediterranean Sea

Abstract

Population structure and biogeography of marine organisms are formed by different drivers than in terrestrial organisms. Yet, very little information is available even for common marine organisms and even less for their associated parasites. Here we report the first analysis of population structure of both a cephalopod host (Sepia officinalis) and its dicyemid parasite, based on a homologous molecular marker (cytochrome oxidase I). We show that the population of common cuttlefish in the Mediterranean area is fragmented into subpopulations, with some areas featuring restricted level of gene flow. Amongst the studied areas, Sardinia was genetically the most diverse and Cyprus the most isolated. At a larger scale, across the Mediterranean, the population structure of the parasite shows co-diversification pattern with its host, but a slower rate of diversification. Differences between the two counterparts are more obvious at a finer scale, where parasite populations show increased level of fragmentation and lower local diversities. This discrepancy can be caused by local extinctions and replacements taking place more frequently in the dicyemid populations, due to their parasitic lifestyle.

Natural geochemical markers reveal environmental history and population connectivity of common cuttlefish in the Atlantic Ocean and Mediterranean Sea

“…Migrations from natal sites in the Mediterranean Sea to areas in the NEAO occur for highly migratory species such European eel Anguilla anguilla [29] and Atlantic bluefin tuna Thunnus thynnus [30]; however, connectivity between the NEAO and Mediterranean Sea for species assumed to display limited movements is ostensibly uncommon, and this type of egress activity has not been previously reported for S. officinalis. Nevertheless, our observation of S. officinalis of W-MED origin being present in the NEAO proximal to the Strait of Gibraltar is in accord with findings on stock structure using genetic markers, with Drábková et al [28] reporting that S. officinalis from the NEAO and W-MED on each side of this passageway were grouped into the same subpopulation (genetic cluster). Because S. officinalis lays egg clusters that are typically attached to benthic plants or substrate and hatch fully developed [31], their dispersal potential relative to species with pelagic larvae is likely very limited.…”

“…This also indicates that environmental conditions experienced by S. officinalis were distinctive at the regional scale, and possibly associated with population structure. A recent study using genetic markers reported that populations of S. officinalis in the Mediterranean Sea are fragmented into several subpopulations [28], and the geographical areas of their genetic clusters were remarkably similar to our regional resolution using geochemical markers. Interestingly, all of our sampling sites in both the C-MED (G, H, I) and E-MED (J, K, L) were each associated with unique genetic clusters (i.e.…”

“…Similarly, we detected a shift in both cuttlebone δ 18 O CORE and δ 18 O EDGE between these two geographical areas (A, B versus C, D) (figures 4b and 5b). Genetic data also showed that sites on both sides of the Strait of Gibraltar (NEAO = C, D; W-MED = E) were part of the same subpopulation cluster, indicating that gene flow occurs through this corridor [28]. Application of these geochemical markers was also used to investigate exchange of S. officinalis between the NEAO and Mediterranean Sea over a restricted geographical scope.…”

“…Similarly, we detected a shift in both cuttlebone δ 18 O CORE and δ 18 O EDGE between these two geographical areas (A, B versus C, D) (figures 4 b and 5 b ). Genetic data also showed that sites on both sides of the Strait of Gibraltar (NEAO = C, D; W-MED = E) were part of the same subpopulation cluster, indicating that gene flow occurs through this corridor [ 28 ].…”

“…Nevertheless, our observation of S. officinalis of W-MED origin being present in the NEAO proximal to the Strait of Gibraltar is in accord with findings on stock structure using genetic markers, with Drábková et al . [ 28 ] reporting that S. officinalis from the NEAO and W-MED on each side of this passageway were grouped into the same subpopulation (genetic cluster). Because S. officinalis lays egg clusters that are typically attached to benthic plants or substrate and hatch fully developed [ 31 ], their dispersal potential relative to species with pelagic larvae is likely very limited.…”