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Phylogeography and Population Structure of Two Brachistosternus Species (Scorpiones: Bothriuridae) from the Chilean Coastal Desert – the Perils of Coastal Living

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Phylogeography and Population Structure of Two Brachistosternus Species (Scorpiones: Bothriuridae) from the Chilean Coastal Desert – the Perils of Coastal Living Biological Journal of the Linnean Society, 2016, , – . With 1 figure. Biological Journal of the Linnean Society, 2017, 120 , 75–89. With 1 figures Phylogeography and population structure of two Brachistosternus species (Scorpiones: Bothriuridae) from the Chilean coastal desert – the perils of coastal living F. SARA CECCARELLI1*, JAIME PIZARRO-ARAYA2 and ANDRES A. OJANGUREN- AFFILASTRO1 Downloaded from https://academic.oup.com/biolinnean/article/120/1/75/2864989 by guest on 29 September 2021 1Division de Aracnologıa, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Av. Angel Gallardo 470, C1405DJR, Buenos Aires, Argentina 2Laboratorio de Entomologıa Ecologica, Departamento de Biologıa, Facultad de Ciencias, Universidad de La Serena, Casilla 599, La Serena, Chile Received 2 May 2016; revised 22 June 2016; accepted for publication 22 June 2016 Coastal deserts are geologically dynamic areas of the Earth, affected by historical changes in sea levels and in some cases also by fault-line tectonic activity. An example of such a dynamic area is the Chilean coastal desert of the Antofagasta and Atacama regions, which harbours many endemic species, such as the bothriurid scorpion species Brachistosternus paposo and Brachistosternus roigalsinai. In this work, we carry out phylogeographic and population genetic analyses on these scorpions, using two mitochondrial (COI and cyt b) and two nuclear (Actin 5C and wingless) markers to identify species and population structuring, and link these findings to the geological history of the area. The geographical feature separating the two species is identified as the Huasco River, and distinguishing morphological features for these scorpions are presented. Population genetic and phylogeographic outcomes reflect an unstable history across this region for B. paposo and B. roigalsinai, related to sea-level changes affecting coastal habitats, including nearby islands. © 2016 The Linnean Society of London, Biological Journal of the Linnean Society,2017, 2016, 12000, 000, 75–89–000.. KEYWORDS: Chile – eustasy – population genetics – vicariant speciation. INTRODUCTION features have been shaped by a combination of sea- level changes and tectonics (Pedoja et al., 2014). This The desert biome covers about one-fifth of the world’s means that, since the Pliocene, low-lying regions of terrestrial surface and is characterised by extreme present-day coastal areas (including low-elevation environments in which only organisms with specific islands) have been submerged numerous times and adaptations can survive (Mulroy & Rundel, 1977; areas with a shallow sea floor have repeatedly Whitford, 2002; Nagy, 2004). Deserts also provide emerged, thus also joining coastal-shelf islands to spatiotemporal habitat stability for well adapted spe- the mainland. cies (Hartley et al., 2005). Coastal deserts, however, The South American Pacific Coastal Desert (PCD) are an exception to this stability over time, as their of Chile and Peru is an example of a dynamic geo- geographical areas are prone to changes depending graphical area with an extreme environment. The on global sea levels, or eustasy (Carter, 1988). While Chilean coastal desert extends from the Tarapaca to global sea levels during the late Neogene and Qua- the Coquimbo region. The most important rivers ternary periods have been estimated to oscillate by found in this area are, from north to south, the more than 150 m (Haq, Hardenbol & Vail, 1988; Copiapo, Huasco, and the Elqui. The River Copiapo Hardenbol et al., 1998), the shorelines and their has a semi-permanent flow and is an endorheic sys- tem, meaning that it does not drain into the ocean, *Corresponding author: E-mail: [email protected] whereas the Huasco and Elqui rivers have a © 2016 The Linnean Society of London, Biological Journal of the Linnean Society, 2016, , – 1 © 2016 The Linnean Society of London, Biological Journal of the Linnean Society, 2017, 120, 75–89 75 762 F.F. S. S. CECCARELLICECCARELLI ETET AL.AL. PHYLOGEOGRAPHY OF COASTAL DESERT SCORPIONS 3 permanent flow draining into the Pacific Ocean, One of the five major clades of the bothriurid scor- species (about 300 of B. roigalsinai, and 150 of B. MATERIALS AND METHODS which makes them exorheic systems. This area also pion genus Brachistosternus, named the Pacific paposo) were examined during this study to re-estab- contains several continental-shelf islands. To the Coastal Desert Clade (PCDC) (Ojanguren-Affilastro SPECIES LIMITS AND DIAGNOSTIC CHARACTERS lish and evaluate the strength of a new morphological south is the Choros archipelago, which comprises the et al., 2016), is found in the PCD, which is itself an Brachistosternus paposo and B. roigalsinai are consid- diagnostic characteristic, namely the presence of two Choros, Damas, and Gaviota islands. The farthest area of high phylogenetic diversity for this genus ered two distinct valid species based on the species dark spots in the posterodorsal margin of sternite VII from the continent is Choros, which is almost 8 km (Ceccarelli et al., 2016). The PCDC species migrated delimitation analyses of Ojanguren-Affilastro et al. and metasomal segments I–III of B. roigalsinai, which off the coast; next is Damas, about 5 km, and the and speciated along the coast in a general northward (2016; Appendix H). All available specimens of both are absent in B. paposo (see Fig. 1). closest is Gaviota, which is < 1 km off the coast; the direction, from an ancestral area on the central Chi- sea floor between these islands and the coast does lean coast (Ceccarelli et al., 2016). A sister group to not drop below 30 m. Twenty-five km north of the the remaining PCDC species, Brachistosternus Choros archipelago, is Chanaral~ island, located about paposo (Ojanguren-Affilastro & Pizarro-Araya, 2014) 8 km off the coast with an intervening seafloor depth and Brachistosternus roigalsinai (Ojanguren-Affilas- Downloaded from https://academic.oup.com/biolinnean/article/120/1/75/2864989 by guest on 29 September 2021 of about 80–120 m (Aguirre, 1967). Chanaral,~ Choros tro, 2002) inhabit a similar area of the Chilean and Damas islands belong to the Pinguino€ de Hum- coastal desert. No evidence for sympatry has been boldt National Reserve (Sistema Nacional de Areas� found so far in the two species (Ojanguren-Affilastro Silvestres Protegidas del Estado, SNASPE area; Cas- & Pizarro-Araya, 2014), with the geographical limits tro & Brignardello, 2005; see Supporting Informa- thought to be at 26° to 30° for B. roigalsinai (Ojan- tion, Figure S1 of the Supporting Information). Like guren-Affilastro, Mattoni & Prendini, 2007a; Ojan- several other coastal areas, this region has been guren-Affilastro et al., 2007b), and restricted to the affected by constant sea-level changes (Le Roux area of Paposo (approximately at 25°) for B. paposo et al., 2005) coupled with tectonic uplift and associ- (Ojanguren-Affilastro & Pizarro-Araya, 2014). Addi- ated seismic activities caused by the subduction of tionally, the presence of B. roigalsinai has also been the Nazca plate under the South American plate reported from the Choros archipelago (Pizarro-Araya (Kendrick et al., 2003; Husson, Conrad & Faccenna, et al., 2014a), and recently several specimens of this 2012). Such geological events are expected to have species have been collected from Chanaral~ island affected the local flora and fauna populations as (Alfaro, Pizarro-Araya & Mondaca, 2014; Pizarro- well. Araya et al., 2014b); however, the island specimens Population genetic and phylogeographic analyses present slight morphological differences with respect are useful tools for inferring past patterns and pro- to the continental populations, as was found for the cesses of species at the transition between intra- and tenebrionid Praocis (Praocis) spinolai (Ben�ıtez et al., inter-specific levels, which, in the case of extreme, 2014). Based on the results of a recent molecular geographically dynamic areas such as the Chilean study (Ojanguren-Affilastro et al., 2016), the distri- coastal desert, reveal the extent to which this rela- butional limits of the two species have been ques- tive instability affects its inhabitants. Furthermore, tioned, raising doubts about the diagnostic the effect of geographic barriers (such as rivers and characters of both species and the specific identity of the sea separating islands from the mainland) on their populations. genetic structuring can be assessed. Here, a more detailed study of the morphology of Among the South American desert-specialized several populations of B. roigalsinai and B. paposo fauna, several scorpions belonging to the families from their entire distributional range, combined with Bothriuridae, Buthidae, and Caraboctonidae have the data of the species delimitation analysis pre- adapted to living in this extreme environment. Par- sented by Ojanguren-Affilastro et al. (2016), sheds ticularly, the scorpion genus that is most adapted light on the identity and diagnostic characters of and diversified in these areas is Brachistosternus, these two species. Based on these newly inferred spe- belonging to the family Bothriuridae, which occurs cies limits, the phylogeography and population histo- even in the most extreme arid environments of the ries of two bothriurid scorpion species from the continent, such as the Atacama and Sechura deserts Chilean coastal desert, B. paposo and B. roigalsinai (Ochoa, 2005; Ojanguren-Affilastro & Ram�ırez, 2009; are investigated, to answer questions about specia- Kova�r�ık & Ojanguren-Affilastro, 2013; Ceccarelli tion and population
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