Tropical fishes in a temperate sea: evolution of the wrasse Thalassoma pavo and the parrotfish Sparisoma cretense in the Mediterranean and the adjacent Macaronesian and Cape Verde Archipelagos

Abstract

The northeastern Atlantic and the Mediterranean Sea share geological histories and display great faunal aYnities. The majority of the Mediterranean species have Atlantic origins, with a few species with tropical aYnities. These include the parrotWsh Sparisoma cretense and the wrasse Thalassoma pavo that are restricted to the subtropical northeastern Atlantic, the Macaronesian archipelagos (Azores, Madeira, and Canaries) and the southern Mediterranean. The Pleistocene glaciations have been described as having diVerent eVects on the fauna of the two regions. During glacial peaks, Mediterranean waters remained warmer than those of the adjacent Atlantic. Within the eastern Atlantic, the eVects of Pleistocene glaciations were diVerentiated. Here, we perform a comparative analysis focusing on T. pavo and S. cretense populations from the northeastern Atlantic and the Mediterranean to assess the eVects of Pleistocene glaciations in these two species. Sequences from the mitochondrial control region were obtained and analyzed combining phylogeographic and demographic approaches. Gene Xow between Atlantic and Mediterranean populations was shown to be very high. The Mediterranean populations of T. pavo and S. cretense showed high levels of genetic diversity, even in the eastern basin, pointing to an ancient colonization event. This suggests that both species must have been able to persist in the Mediterranean during the cold Pleistocene periods. Historical migration estimates revealed a Mediterranean towards Atlantic trend in the case of T. pavo, which may reXect the re-colonization of areas in the Atlantic by Wsh that survived the cold phases in relatively warmer Mediterranean refugia. Our data also showed that within the Macaronesian Archipelagos, migrations occurred from Madeira towards the Azores, for both T. pavo and S. cretense, thus supporting a post-glacial colonization of the Azores by Wsh that persisted in the warmer region of Madeira. Similar geographic distributions, thermal aYnities, and means of dispersion for T. pavo and S. cretense resulted in a similar response to the eVects of Pleistocene glaciations, as evidenced by identical phylogeographic patterns.

Pliocene and Late Pleistocene actinopterygian fishes from Santa Maria Island, Azores (NE Atlantic Ocean): palaeoecological and palaeobiogeographical implications

“…Our view differs from that of previous authors, who suggested that 'the drop of sea temperatures : : : that occurred during the Pleistocene probably resulted in mass extinctions' (of fishes) and so 'most of the organisms now present would have reached the Azores in the last 17,000 years' (Santos et al 1995). Our reasoning also contradicts the conclusions of Domingues et al (2008), who stated that 'persistence of : : : S. cretense in the Azores archipelago during the Pleistocene glaciations is difficult to admit'. Moreover, the very abundant and well-studied MIS 5e (i.e.…”

“…The finding of fossil pharyngeal plates belonging to S. cretense in MIS 5e sediments does not necessarily preclude the hypothesis that this species locally disappeared during the Last Glaciation, only to recolonize the archipelago post-glacially. Nevertheless, we consider it more plausible to argue that such extirpation did not happen, taking into consideration the facts that: (1) detailed studies on the Azorean MIS 5e and recent marine molluscs showed that the drop of the SSTs during the Last Glaciation only affected two groups of species: the tropical species that reached the Azores probably during a 'window of opportunity' associated with the final phase of Termination 2, and bivalve species associated to fine-sand sediments; both groups were extirpated (Ávila et al 2008a, b, 2009b, 2015b); (2) as temperature is known to play a key role on marine fish species biology (Pepin, 1991;van der Kraak & Pankhurst, 1997;Pankhurst & Porter, 2003;Dolomatova et al 2013;Poloczanska et al 2016) and, in light of previously published theories (Ávila et al 2008a, 2009b, 2015b), the drop of SSTs was not sufficient enough to severely affect the survival, growth and reproduction of the temperate parrotfish S. cretense in the Azores during the Last Glacial episode; and (3) if S. cretense was a post-glacial colonizer of the Azores, the genetic diversity of the Azorean populations should be low in comparison to southern Madeiran populations (postulated to have been unaffected by the drop of SSTs); that is not the case, however, as pointed out by Domingues et al (2008). Combining our palaeontological data with ecological and genetic data from other authors (Abecasis et al 2008;Afonso et al 2008;Domingues et al 2008), we therefore believe the most plausible scenario is the survival of most (if not all) temperate and subtropical fish species in the Azores during the Last Glacial episode, as long as their ecological traits were not constrained to sandy habitats.…”

“…This study therefore aims to: (1) review and update the status of all existing Actinopterygii fossil material from Santa Maria Island; (2) use this new data to test previous statements by several authors (e.g. Briggs, 1974;Santos et al 1995;Domingues et al 2006Domingues et al , 2008 who concluded that the shallow littoral fauna of the Azores was extirpated during the Last Glacial episode; and (3) compare the palaeobiogeographical and palaeoecological patterns known from sessile and low-dispersive species (e.g. non-planktotrophic marine molluscs) with that of highly motile species such as fishes.…”

Mitochondrial DNA reveals Pleistocenic colonisation of the Mediterranean by loggerhead turtles (Caretta caretta)

“…Nevertheless, the presence of haplotype CC-A6.1 in Western Greece and haplotypes CC-A3.2 and CC-A52.1 in Eastern Turkey indicates that these populations might have survived at least the most recent glacial peak. Consequently, the northern part of the Eastern Mediterranean and Western Peloponnese seems to have acted as warm refugia for marine species at that time, as has already been suggested for fishes (Domingues et al, 2008). This hypothesis could explain the genetic structure currently seen in Turkey, with a strong westward decline in haplotype diversity and a high variability in the frequency of CC-A3.1 between adjoining sites.…”

Phytogeography ofLusitanianMacaronesia: biogeographic affinities in species richness and assemblage composition

“…These archipelagos share similar geomorphological traits; they are all volcanic in origin, and although there is no general consensus, most are thought to be the result of several geologic hotspots (Carracedo, 2001). They have a unique biogeography: all native flora and fauna reached the archipelagos via long-distance dispersal from adjacent continental areas (Whittaker & Ferna´ndez-Palacios, 2007) or, in some circumstances, adjacent archipelagos (Domingues et al, 2008). Marine biotas of the different archipelagos are interconnected via oceanic currents; surface currents generally (but not always) move from the Azores towards Madeira and the Canary Islands (Morton et al, 1998).…”