Unveiling the unknown phylogenetic position of the scallop Austrochlamys natans and its implications for marine stewardship in the Magallanes Province
This is the first comparative study of commercial scallop species in the Pacific coast of the MP combining morphological and molecular characters. Our phylogenetic analyses highlight the association between A. natans and Ad. colbecki; two members of monospecific tribes and last extant representatives of their Southern Ocean-restricted genera.These results confirm the presence of both Magallanes scallops in the MP, as well as the so-far unsuspected presence of mixed “banks” where both species occur in sympatry. The BND/VH ratio helps discriminate between two distinct entities that belong to the genetic lineage of Z. patagonica and to a different lineage, highly divergent from the former, which corresponds to A. natans. A. natans is the only species of a whole lineage with a particular phylogenetic value, therefore having developed and tested an accurate identification criterion for both scallops will allow efficient fishery management in the future.Here we discuss the phylogenetic position and the taxonomic status of both Magallanes scallops, as well as the implications of these results for the future management and conservation of Z. patagonica and A. natans in the Magallanes Region. Despite the numerous classifications built on morphological, ecological or molecular data, the relationships among pectinids are still under constant modification depending on the number of taxa, loci, length of the sequence and the selected outgroups1,4. The work of Alejandrino et al.7 is the most inclusive so far in terms of taxon sampling, with 81 species. Although Scherrat et al.25 included 143 species, the node supports of the phylogenetic trees are not provided, making it difficult to assess the robustness of this large phylogeny. In order to define the phylogenetic position of Zygochlamys patagonica and Austrochlamys natans, we included 93 pectinid taxa (43 genera) representative of tribes Chlamydini, Crassadomini, Fortipectini, Palliolini, Aequipectinini, Pectinini and Amussini. Comparing to Waller’s5 and Dijkstra’s15 classifications, only the subfamily Camptonectinae and the tribe Mesoplepini are missing. We used three ribosomal regions (one nuclear and two mitochondrial). Compared to Alejandrino et al.7, histone H3 is missing here, however this locus is among the least informative4. The family Pectinidae appears to be monophyletic with high support values (Fig. 5, S2), as previously demonstrated4,7,26,27,28. According to Dijkstra15 there are currently five subfamilies of Pectinidae, two of which are absent from our analysis: Camptonectinae and Pedinae. This topology supports the classifications of Waller5 and Dijkstra15, except for the position of the tribe Austrochlamydini.Our Magallanes scallops separated into two very divergent clades: Z. patagonica is associated with its conspecifics and congenerics in a single lineage (Fig. 5), which also contains species of Veprichlamys and Talochlamys. This lineage already appeared well supported as the sister clade to Palliolinae and Pectininae in Alejandrino7. For the first time, Talochlamys dichroa and T. gemmulata are nested with high support values into the Zygochlamys clade, making this latter genus paraphyletic (Fig. 5). These taxa are all restricted to high latitudes of the Southern Ocean. Due to phylogenetic and geographic affinities, we suggest that these three genera may constitute a tribe separate from Chlamydini. Since Dijkstra15 moved the two Atlantic ‘Crassadoma’ into the genus Talochlamys, the affinities among Talochlamys spp. had not been explored until now. Talochlamys species rather associate according to geographic affinities, splitting the genus into two highly divergent entities corresponding to European and New Zealand Talochlamys. A systematic revision of these four species would be useful.Austrochlamys natans associated with the Palliolinae, which was elevated to a subfamily rank by Waller5. Of the three extant tribes that compose this group, Mesopleplini are missing from our phylogenetic analyses. We included 4 genera (8 species) of the remaining two tribes: Adamussium (Adamussini) and Palliolum, Pseudamussium, Placopecten (Palliolini). The present sampling of Palliolini is the most inclusive to date and led to the monophyly and full support of the tribe Palliolini. Our phylogenetic results do not support any of the previous classifications of the tribe Austrochlamydini1,5,9,13,15, and introduce this monospecific tribe as a new member of the subfamily Palliolinae. Indeed, Austrochlamys natans clusters together with Adamussium colbecki, both in a sister clade to Palliolini. The first molecular characterization of Ad. colbecki did not lead to a clear classification due to the low polymorphism of the 18S26. Later, Ad. colbecki appears either as sister species to Chlamydinae or to Palliolini, depending on tribe sampling and the choice of outgroup and loci4,10,11. However, in the most recent and inclusive studies of taxon sampling7 (present study) or genomic cover29, Ad. colbecki is the sister group of the tribe Palliolini, as in the present phylogeny.The subfamily Palliolinae originated from a Chlamydinine ancestor in the Cretaceous and subsequently underwent diversification in the Northern Hemisphere1 and in the Southern Hemisphere, where the extinct genus Lentipecten spread in the Paleocene–Eocene Thermal Maximum30. The genus Adamussium derived from Lentipecten and appeared in the early Oligocene; it comprises 5 endemic Antarctic species; Ad. colbecki is the only one extant13,31,32. The genus Austrochlamys also appeared in the Oligocene and was first restricted to King George Island (South Shetlands), then spread around the north of the Antarctic Peninsula and achieved a circum-Antarctic distribution until the Pliocene13,33,34. Austrochlamys persisted during the progressive cooling of the Antarctic Continent from the Paleocene to the Pliocene, dominating the coastal areas, while Adamussium occupied the deep seas and continental platform33. The opening and deepening of the Drake Passage and the intensification of the Antarctic Circumpolar Current during the Pliocene provoked a drastic cooling and the extension of sea ice over the coastal habitat, which caused the northward movement of Austrochlamys and its subsequent disappearance from Antarctica, along with the circumpolar expansion of Ad. colbecki in Antarctic shallow waters33. The colonization of the coastal habitat has been related to the sea ice extent that provided a more stable environment and low-energy fine-grained sediment with which Adamussium was associated in the deep waters. Austrochlamys fossils appear in the Subantarctic Heard Island in late Pliocene layers (3.62–2.5 Ma35). Today Ad. colbecki is a circum-Antarctic and eurybathic species that reaches high local density in protected locations13,36, while all Austrochlamys became extinct except for A. natans, which is restricted to southern South America33. The phylogenetic affinity highlighted here between A. natans and Ad. colbecki has its origins in the Southern Ocean; the deep divergence between the lineages of these monospecific tribes attests to the long time since their common origin in the Paleogene. These results point out both species as relevant biogeographic models to address longstanding questions regarding the origin of marine biota from Southern Ocean.The nomenclature, taxonomy and ecology of both A. natans and Z. patagonica have been problematic for almost 200 years. Since its original description37, Z. patagonica, a.k.a. the “Ostión Patagónico” has been named with more than 10 synonyms, probably due to the great intra-specific morphological variability throughout its distribution19,38 (see the nomenclatural history in Supplementary Table S1). In contrast, there are very few records in the scientific literature and no genetic data on A. natans, a.k.a. the “Ostión del Sur”13,14,17,19, and some problems of nomenclature and establishing diagnostic characters persist since its description13,39. Many of the current junior synonyms of both species were described from small and juvenile specimens (under 52 mm VH39,40,41). Indeed, all deposited type material of A. natans ranges from 23.5 to 52 mm VH; the latter is half of the maximum size39. The criteria most commonly used for the identification of both scallops were number of radial primary ribs, maximum size, shell colour and presence of laminated concentric lines (Supplementary Table S1). Specimens with marked primary and secondary radial ribs alternated regularly and more whitish colouring of the right shell were attributed to Z. patagonica, while those with weaker and less markedly coloured radial ribs and the maximum size were considered as A. natans42. However, the number of radial ribs overlaps between Z. patagonica (26–4212,43) and A. natans (22–5017,19). These characters also have high variability across different environments and during ontogeny13,17. Thus the use of a taxonomy based on environment-sensitive and allometric characters has led to confusion in the morphological identification of these species13,38. The criterion used in the present study, the BND/VH ratio established by Jonkers13, discriminates the species efficiently. As attested by the narrow dispersal cluster in Fig. 3, this character has low intra-population variability13. In some cases a level of intraspecific variation can be detected, and this is mainly due to the environments where the scallop populations inhabit19 (e.g. exposed, protected, substrate type, fjord, oceanic). However, although there may be some intraspecific variability between populations, this variability does not generate problems for the identification of the two species. Individuals of A. natans generally presented a significantly greater BND/VH ratio than those of Z. patagonica. However, it is important to consider that, given that this character varies during ontogeny, it is more accurate in individuals over 25 mm VH13. Only the molecular identification was able to discriminate juvenile scallops of both species accurately.According to the literature, A. natans is restricted to interior waters of channels and is associated with kelp forests of M. pyrifera (Supplementary Table S1). Z. patagonica inhabits a wider range of environments such as bottoms of shells, sand, mud and gravel in protected and exposed areas, between 2 and 300 m depth (Supplementary Table S1), but is also associated with kelp forests in fjords with different degrees of glacial retreat12,16,44. The juveniles of both scallops recruit in kelp forests44,45. According to the local artisanal fishermen, adults of “Ostión del Sur” (A. natans) occur in fjords with glaciers (orange circles in Fig. 123). We included two sampling locations near glaciers (in Pia and Montañas fjords), where large individuals (between 46 and 86 mm) of A. natans and Z. patagonica occur in sympatry. This sympatry was previously reported in Silva Palma Fjord between 5 and 25 m depth16. In conclusion, scallop banks are not monospecific but rather mixed and Z. patagonica occurs in the interior waters of the channels and fjords. Consequently, these two species have overlapping ecology (recruiting zone and glacial affinity) in the channels and fjords, overturning a long-held view that these scallops have marked habitat segregation.The fishery for both species was established in the 1990s in the political-administrative Region of Magallanes16, despite the complexity of the morphological recognition of scallops. The distinction between species was based on shell colour and radial ribs42, two characters that, given the results of this study, do not have this diagnostic capacity. Consequently, the scallop fisheries in the Magallanes Region are currently based on inaccurately discriminative characters. Scallop banks in MP have always been considered as monospecific16,47. A great part of scallop landing has always been attributed to A. natans47, about which the scientific literature is scarce (Supplementary Table S1). Conversely, Z. patagonica, which was erroneously considered as the commercial species of southern Chile, has more scientific research (Supplementary Table S1).The difficulty to discriminate A. natans and Z. patagonica morphologically may lead to incorrect fishery statistics and uncertain conservation status of A. natans. Incorrect fishery statistics could overestimate the abundance of banks of A. natans compared to Z. patagonica. If the minimum catch size is reduced23 in the context of the fishing overuse of the last decade, A. natans may suffer a reduction of its maximum size48. Therefore, an identification criterion between species is a need to improve fishery management. We showcased a quantified criterion that is useful to identify both species. In the short-term, this method can be used, but it is difficult to enforce in practical ways. We suggest to train fishing inspectors, following three guidelines. First, the identification should consider only the right valve (RV) for species identification, since the left valve is not taxonomically informative. Second, for visual classification, check the outline of the BN, mainly because the individuals of Z. patagonica have a more arcute BN. Third, a reliable identification has to measure the depth of the byssal notch (BND) and shell height (VH) ratio. Lastly, future research and fishery monitoring should follow these criteria to carry out a correct identification and subsequently better landings statistics.Molecular tools allowed evaluating the phylogenetic relationships of scallops globally or regionally and incorporating parameters that can be used for the management and conservation of species of commercial interest49. For example, in the last few decades metrics have been developed to address conservation problems that give us a measure of the current state of particular taxa. These conservation priorities are often seen as measures for threatened species categorized by the IUCN Red List (World Conservation Union, 1980), one of the most widely and recognized systems. Although this prioritization metric incorporates phylogenetic distinctiveness (PD), this factor has been updated due to the importance of quantifying the loss of evolutionary diversity that would be implied by the extinction of a species50. The magnitude of the PD loss from any species will depend (but not exclusively) on the fate of its close relatives51. The “Ostión del Sur”, Austrochlamys natans is the last representative of its tribe (Austrochlamydini) in the Southern Ocean. Its phylogenetic position and the long branch length (i.e. the length of the branch from the tip to where it joins the tree), which represents an important amount of evolutionary change, highlights the degree of isolation of A. natans and calls attention to the possible loss of a unique genetic lineage. There is currently no conservation value for this relict species; we sought to alert the current fishery management that the “Ostión del Sur” is a distinct taxon and provide integrative evidence for further conservation studies.Finally, regarding the overlapping niche of these scallops and the conservation importance of the clade of A. natans, we propose three key recommendations for the future scallop fishery policies in the sub-Antarctic channels. First, it is necessary to assess the proportion of both species per bank and landing to generate a distribution map through the sub-Antarctic channels. For this assessment, the byssal notch depth is the most appropriate morphological character. Second, we recommend reassessments of biological and ecological parameters (e.g. size at first maturity) for A. natans across the glacial fjords, which are the most relevant fishing sites. As a final point, today there is a complete lack of knowledge of the genetic connectivity along the Subantarctic Channels. Thus we should generate more research about spatial population genetics at different temporal scales. The integration of genomic approaches (e.g. SNPs) with macro- and micro-environmental modelling approaches provide enormous opportunity to establish a new regional zoning for fishery management and conservation scallop strategy. More
