Past climate fluctuations are known to have influenced the distribution of many species (Hewitt, 2000), as well as their population genetic structure (Collin and de Maintenon, 2002; Taylor and Hellberg, 2006). The late Pleistocene presented alternating glacial and interglacial periods which had an impact on a global scale (Mackensen, 2004) and shaped the geographic distribution and diversification of several marine organisms, especially within coastal and benthic habitats (Bennett, 1990; Thatje et al., 2005). Glaciations during the late Pleistocene induced changes in the distribution of pinnipeds, such as the South American fur seal (Arctocephalus australis), and the South American sea lion (Otaria byronia) (Túnez et al., 2013, 2010; Oliveira et al., 2017). Changes in the geographic range of southern elephant seals (Mirounga leonina) during the Holocene are thought to have been driven by similar processes (de Bruyn et al., 2009). Such climatic and oceanographic variations have also influenced the current distribution patterns of cetacean species. For example, demographic inference based on mitochondrial DNA (mtDNA) suggests that after glacial events during the Pleistocene white-beaked dolphins (Lagenorhynchus albirostris) expanded into the North Atlantic (Banguera-Hinestroza et al., 2010). In a similar manner, it has been shown that the population expansion of beluga whales (Delphinapterus leucas) into the western Nearctic and their dispersal routes from glacial refuges relates to the retreat of the Pleistocene ice cover (O’Corry-Crowe et al., 1997).

Climatic variations have also shaped the distribution and genetic population patterns of dolphins in the genus Cephalorhynchus. This genus comprises four small-sized species which live in coastal, temperate to subantarctic waters around the Southern Hemisphere (Dawson, 2018). According to the radiation model proposed for this genus, speciation was promoted by periods of changing climate, and followed the direction of the West Wind Drift, ultimately giving rise to the current discontinuous distribution of the four recognized species (Pichler et al., 2001). This process is thought to have started in southern Africa, where presently Heaviside’s dolphins (C. heavisidii) occur off the west coast of South Africa and Namibia. Subsequently, Cephalorhynchus arrived at the inshore waters of New Zealand, giving rise to Hector’s dolphins (C. hectori) and later diverging into two subspecies, C. hectori hectori in the South Island and C. hectori maui in the North Island (Baker et al., 2002). The radiation process of the genus continued eastward across the South Pacific, arriving at southern South America (SA) where there are now two recognized species, the Chilean dolphin (C. eutropia) and the Commerson’s dolphin (C. commersonii). Chilean dolphins inhabit the coastal waters of central and southern Chile, from Valparaíso to Isla Navarino (Goodall, 1994) and a few have also been documented on the Atlantic coast at Puerto Deseado, Argentina (Morgenthaler et al., 2014). Their current genetic structure along the Chilean coastline is consistent with predictions from the Expansion-Contraction biogeographic model with a poleward post-glacial shift (Pérez-Alvarez et al., 2016).

Commerson’s dolphins are mainly found along the coast of Argentina south to the central and eastern Strait of Magellan, and the Falkland Islands/Islas Malvinas (FI/IM) (Brownell and Praderi, 1985; Dawson, 2018). It has been suggested that Commerson’s dolphins in the latter region might have diverged significantly from their conspecifics off SA, even corresponding to a separate subspecies (Cipriano et al., 2011). Commerson’s dolphins are also found 8,500 km away from SA, in the coastal waters of the subantarctic Kerguelen Islands (KI) in the southern Indian Ocean (Dawson, 2018). This wide gap in distribution is in marked contrast with the distribution of the other Cephalorhynchus species and makes the geographic range of C. commersonii the broadest in the genus (Goodall et al., 1988). In addition to the conspicuous geographical distance between SA and KI, morphological and coloration differences (Robineau, 1984) as well as acoustic differences (Dziedzic and De Buffrenil, 1989) have been noted between individuals of both areas. Some of these lines of evidence led to a subspecies proposal (Robineau, 1986) and a subsequent formal description as C. c. kerguelenensis, based on morphological, skeletal and genetic characters (Robineau et al., 2007). Following the diversification model proposed for the genus, C. c. kerguelenensis is thought to have originated around 10,000 years ago through the establishment of a few migrants from SA (Pichler et al., 2001), akin to a long-distance dispersal and an establishment model (as defined by Crisp et al., 2011). This model represents an allopatric speciation process, originating with an exceptional dispersal event, from which a new population then establishes across a barrier at a sufficient distance to limit gene flow between the two populations (Crisp et al., 2011). Since the subspecies description, additional studies of the genetic diversity of C. commersonii have been conducted along the southern Argentine coast (Pimper et al., 2010; Cipriano et al., 2011). However, no further investigation has been conducted on the population genetic structure over the complete distribution of the two subspecies.

To explore the establishment of C. commersonii in the KI and to test whether genetic data support the proposed long-distance dispersal and establishment model, we designed a geographically extensive, balanced sampling scheme throughout the global distribution of Commerson’s dolphins using new and published mtDNA control region sequences. We included samples from the previously unsurveyed areas of FI/IM, southern Chile (Fitzroy), Argentina (Bahía Camarones, Punta Quilla, and Monte León), new samples from Puerto Deseado (Argentina), and additional samples from the KI. To complete a general phylogeographic overview of the species, we combined this new information with published sequences from the Strait of Magellan, Tierra del Fuego (Argentina), and the KI.

A geographically extensive sampling scheme, including both new and previously published sequences of the mtDNA control region, allowed us to estimate the genetic diversity and genetic structure across the entire range of the Commerson’s dolphin. From this, we evaluated the previously proposed establishment hypothesis of the KI population (Pichler et al., 2001) as a long-distance dispersal model (Crisp et al., 2011).

The genetic diversity indices we obtained for continental SA are similar to results from previous work conducted in this area. Along the southern Argentina coast, from Puerto Deseado to the Strait of Magellan (n = 57), Cipriano et al. (2011) found 11 haplotypes and a genetic diversity of Hd = 0.671. Further south, along the coast of Tierra del Fuego (n = 196), Pimper et al. (2010) found 20 haplotypes and Hd = 0.807, although many of the latter samples are also used in our study. Our genetic and phylogeographic structure results were also similar to those of Cipriano et al. (2011), showing genetic structure over similarly short distances (Table 2). In the absence of physical barriers along the Argentine coast, behavioral or environmental barriers have been suggested as drivers for this genetic structure (Pimper et al., 2010; Cipriano et al., 2011), as in studies on other species in the genus. In the sister species C. eutropia, strong mitochondrial and nuclear genetic differentiation between north and south populations has been described in the absence of physical barriers along the Chilean coast (Pérez-Alvarez et al., 2015) and coincides with the boundary of two recognized biogeographic provinces of the Southeastern Pacific (Camus, 2001; Escribano et al., 2003). The Chilean dolphin has also shown short movements along the shore (mean 23.1 km) and reduced home ranges (Heinrich, 2006). Similarly, along the South African coast, Heaviside’s dolphins also exhibit genetic population structure across short distances (Gopal et al., 2019). Such small scale genetic structure may be related to reduced home ranges as detected during tracking period of 54 days in C. heavisidii females (Elwen et al., 2006). Finally, Hector’s dolphins show genetic structure over distances as short as 100 km (Hamner et al., 2012), limited along-shore movements (average of 31 km) (Bräger et al., 2002) and display site fidelity and reduced home ranges (Bräger et al., 2002; Rayment et al., 2009).

In addition to exhibiting genetic structure within areas with no obvious barriers, Hector’s dolphins also present marked genetic and phylogeographic structure over areas with potential dispersal barriers, such as the Cook Strait, which separates New Zealand’s North and South Islands (Baker et al., 2002; Hamner et al., 2012). In this latter case, combined genetic and morphologic evidence led to the description of two different subspecies, C. h. hectori, also referred to as the South Island Hector’s dolphin; and the critically endangered C. h. maui exclusively found off the West Coast of the North Island and known as the Mâui dolphin (Baker et al., 2002). SA and the FI/IM are separated by 400–550 km of open ocean at their closest point, much more than the 20 km that separate New Zealand’s North and South Islands. In contrast to C. h. hectori and C. h. maui, Commerson’s dolphins from populations along the SA coast and the FI/IM share several haplotypes (Table 1) and do not show high levels of genetic differentiation (Table 2). The net nucleotide divergence between FI/IM and SA of d_A = 0.051% is an order of magnitude below the lower subspecies threshold suggested for cetaceans (d_A = 0.4%) (Taylor et al., 2017). Furthermore, the migration analysis suggested moderate migration rates between SA and the FI/IM. The estimated number of effective migrants fits within the range of one to four, which may indicate a migration-drift equilibrium between these two regions. Alternatively, some degree of isolation may be occurring between the FI/IM and SA populations. On one hand, the low diversity in FI/IM may suggest a past founder effect after a possible migration from SA. On the other hand, the low but significant phylogeographic structure may also suggest an incipient divergence between them. In this context, the several haplotypes shared between these regions would be explained by slow linage sorting related to their population sizes. However, based on the recognized, currently accepted, consensus criteria, Commerson’s dolphins of SA and the FI/IM lack enough genetic distinctiveness to be considered different evolutionary units. These results contribute genetic data on a cetacean species to the body of information which supports grouping the FI/IM into the same biogeographic province as SSA (>40°S), the Magellanic biogeographic province (Cousseau et al., 2019). Even if these results are based on a single mitochondrial marker, they suggest that female-mediated gene flow between the two areas did occur at least until recently, which is also supported by the presence of several shared haplotypes. Commerson’s dolphins are capable of occasionally traveling long-distances, which makes continued movements between SA and FI/IM possible. They have been recorded over 180 km out at sea in waters over 1,000 m in depth (Pedraza, 2008), as far out as the Drake Passage (Aguayo, 1975) and off the coast of South Africa (de Bruyn et al., 2006). In this genus, such ventures are not exclusive to Commerson’s dolphins; long-distance movements exceeding 400 km over deep waters have also been described for Hector’s dolphins (Hamner et al., 2014). Nevertheless, these long-range movements are considered unconventional for Commerson’s dolphins, as most records lack proper evidence and are speculative (Brownell and Praderi, 1985; van Waerebeek et al., 2010).

The 8,500 km gap in distribution range of C. commersonii, between SSA, the FI/IM, and the KI (Dawson, 2018), is the widest gap for this genus and presents a potentially significant barrier to dispersal. Previously described osteological, morphological, acoustic and genetic differences between dolphins from these two distant regions (Robineau, 1986; Dziedzic and De Buffrenil, 1989; Robineau et al., 2007) lead to them being considered two subspecies, C. c. commersonii and C. c. kerguelenensis. In relation to previous studies (Robineau et al., 2007; Pimper et al., 2010; Cipriano et al., 2011), here we present a geographically broader sampling scheme, including new areas like Fitzroy, Chile, and the FI/IM, while increasing sampling size in the KI. This allowed us to contribute a fuller picture of the global phylogeography of the species. The phylogeographic structure values between the two subspecies (Φ_ST = 0.524–0.655) are well above the next highest value (Φ_ST < 0.39), found between the northernmost locality of Bahía Camarones and FI/IM, i.e., between C. c. commersonii populations (Table 2). The detection of a phylogeographic signal between the samples corresponding to each subspecies by PERMUT further supports this, as well as the results obtained with Lamarc. All migration estimates involving the KI (i.e., samples from the range of C. c. kerguelenensis) were generally much lower than one effective migrant per generation, far below the minimum number to avoid divergence between population. The presence of a single haplotype (H6) shared at very low frequency by KI and SA, as well as the other private haplotypes closely related to H6, may reflect a founder effect followed by the isolation of the colonizers, establishing a newly isolated population. The small population size of the KI population may also have accelerated the lineage sorting process, as observed between Hector’s and Maui’s dolphins in New Zealand (Baker et al., 2002; Hamner et al., 2012). Finally, the net nucleotide divergence of d_A = 0.396% is within rounding error of the recommended interval for the sub-species classification of d_A = 0.4–2.0% (Taylor et al., 2017) and is thus consistent with the current subspecies ranking. The obtained d_A complements the previously described morphological differences between Commerson’s dolphins from SA and the KI (Robineau et al., 2007). Future work could explore the second criterion of diagnosticability (Taylor et al., 2017) using genetic data, such as nuclear markers. In this regard, the KI subspecies may be considered as an incipient, divergent clade of C. commersonii. Pichler et al. (2001) proposed a model of evolution for this genus in which a long-distance dispersal event from South Africa would have permitted the establishment of a new population in New Zealand, which further evolved to C. hectori. In a same manner, a small group of C. hectori would have reached SA, giving rise to both C. eutropia on the Pacific side and C. commersonii on the Atlantic. In this context, C. c. kerguelenensis may represent the most recent and ongoing step in the diversification of Cephalorhynchus, where isolation from their source population is driving an incipient process of future speciation.

All haplotypes obtained from new sequences were deposited in GenBank under the accession numbers OL452036-OL452049 and OL624846-OL624872.

The animal study was reviewed and approved by the Undersecretariat for Fisheries and Aquaculture permits RES 665/2009, RES 67/2010, and RES 334/2012, approved by the Bioethical Committee at the Universidad de Chile. Administración de Parques Nacionales (APN) de Argentina. Oregon State University permit IACUP 4671 licensed by the Government of the Falkland Islands/Islas Malvinas. Permit order n°2013-109, issued by le préfet, administrateur supérieur des Terres australes et antarctiques françaises.

MP-A, RM, CB, PT, CG, AV, PB, MC, EC, CO, and RL: sample collection. MP-A, EP, and SK: contributed reagents, materials, and analysis tools, conceived and designed the analysis, analyzed the data, and wrote the manuscript. SK, MP-A, AV, and DS: laboratory work. MP-A, SK, AV, DS, CD, and RL: acquisition of data. SK: elaboration of figures and tables. All authors read, edited, commented, and approved the final manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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