Haminoea orbignyana

Turani, Martina, Valdés, Ángel & Malaquias, Manuel António E., 2024, Molecular phylogeny of the marine snail genus Haminoea (Gastropoda, Cephalaspidea): A framework to study marine diversity and speciation, Zoologica Scripta 53 (1), pp. 52-77 : 68-70

4.1 | The Haminoea orbignyana – alfredensis – antillarum complex

Probably, the most surprising result of this study is the hypothetical conspecificity of the Eastern Atlantic and Mediterranean Sea species H. orbignyana , with H. alfredensis from the temperate Indian Ocean shores of South Africa, and the Western Atlantic lineages of H. antillarum (groups 15 and 16). Despite the fact that our phylogenetic analyses (Figure 1) rendered these four lineages monophyletic, the genetic distances among them are comparatively lower varying between a minimum of 2.4% ( H. alfredensis and H.orbignyana ) and a maximum of 4.5% ( H. antillarum group 16 and H. orbignyana ), with the genetic distance between the two lineages of H. antillarum estimated at 3.9%. These four lineages are only supported by the COI gene, whereas the 12S and 28S genes rendered support for the clade containing the specimens of H. antillarum from Yucatan (group 15), and the latter gene also provided support for the clade with specimens of H. alfredensis (Figure 1, Appendices S2, S3, S8, S10, S11 and S11). None of the four lineages was supported by the 16S gene analysis, which nevertheless clustered all representatives together but with low node support (PP = 0.72).

The species H. orbignyana , H. antillarum and H. alfredensis are well established in the literature, yet they were never studied in a comparative framework. A closer look at the literature together with our own preliminary data on the morphology of specimens reveals that all these nominal species share a pear-shaped smooth shell and a body colouration characterized by dense black pigmentation along the edges of the cephalic shield and parapodial lobes. In contrast, H. antillarum has mildly denticulated inner lateral radular teeth, whereas in H. alfredensis and H. orbignyana these teeth are smooth. Likewise, whereas in the latter two species, the proximal lobe of the prostate is wider, conferring the prostate an acorn-like shape, in H. antillarum seems to be the opposite with the distal lobe wider compared to the proximal one ( Gosliner, 1987; Macnae, 1962; Malaquias & Cervera, 2006; Marcus & Marcus, 1967; Thompson, 1981; Valdés et al., 2006; personal observations), but this requires further anatomical investigations in order to be confirmed.

Even if our molecular results based on the species delimitation analyses and genetic distances suggest the occurrence of a single ubiquitous species with amphi-Atlantic distribution encompassing the Iberian Peninsula, the Mediterranean Sea, West Africa including the Canary Islands, the temperate shores of South Africa in the Indian Ocean and the western Atlantic along the Yucatan Peninsula, Florida and Bermuda, this warrants caution and further corroboration by conchological and morpho-anatomical data. As highlighted above, H. antillarum seems to be characterized by relevant anatomical differences from the digestive and reproductive systems, and even if genetic distances are comparatively low, this could be due to different evolutionary rates between species of Haminoea .

On the contrary, and even in the absence of sound data on the duration of the pelagic larval stage of Haminoea ( Schaefer, 1996) , the confirmed occurrence of specimens attributed to H. elegans (group 18) on both sides of the Atlantic (Figure 1; only 0.3% different in the COI gene; Table 2) supports a high dispersal capability, at least in some species of the genus ( Martínez & Ortea, 1997; current study as H. ‘ elegans 1’ [group 18]; Figure 1). Thus, we cannot discard that representatives of the orbignyana - alfredensis - antillarum complex may have larvae with high dispersal capability favouring gene flow between distant populations. However, we must admit that the genetic distance between the two putative lineages of H. antillarum from nearby locations, namely the Yucatan side of the Gulf of Mexico (group 15) and the Florida Keys/Florida Peninsula– Bermuda (group 16), estimated at 3.9% and 14 substitutions between these two haplogroups (Figure 3) challenges this view. Even if the prevalent ocean current system in the area suggests putative connectivity between Yucatan and the Florida Peninsula through the Loop Current ( Gyory et al., 2011), faunal breaks between tropical Florida and the more temperate/sub-tropical Gulf of Mexico have been documented for several groups of molluscs and fish ( Briggs, 1974; Lee & Ó Foighil, 2004; Mikkelsen & Bieler, 2000; Reeb & Avise, 1990), likely reflecting seasonal changes in the current systems and water temperatures oscillations. These factors may hinder gene flow between the Yucatan and the Florida– Bermuda populations, creating periods of temporary isolation that could explain the observed genetic discontinuity.

Another interesting aspect is the sister relationship between the lineages H. orbignyana (Eastern Atlantic) and H. alfredensis (temperate South Africa). The cold water of the Benguela current established at the end of the Miocene ( Siesser, 1980) is regarded as a strong barrier for temperate and tropical marine coastal species isolating the faunas of the Atlantic and Indian Oceans, while at the same time, paleontological and morphological evidence suggests that this barrier was sporadically bridged by several coastal invertebrate organisms ( Briggs, 1995; Vermeij & Rosenberg, 1993). Few molecular evidence for dispersal from the Atlantic into the Indian Ocean is still available. This is the case for reef fish ( Floeter et al., 2008; Rocha et al., 2005) and sea slugs ( Churchill et al., 2014; Golestani et al., 2019), which seem to have taken advantage of the disruption of the Benguela and Agulhas currents during warmer interglacial periods of the Pleistocene. Because Haminoea is a genus of Atlantic and Eastern Pacific affinity, the sister relationship between H. orbignyana and H. alfredensis is more parsimoniously explained as being the result of dispersal of larvae or H. orbignyana into the Indian Ocean during these warmer periods, with the establishment of viable populations followed by isolation after the reestablishment of the current system.