Sphyrna tiburo

Ochoa-Zavala, Maried, Mar-Silva, Adan Fernando, Pérez-Rodríguez, Rodolfo, Palacios-Barreto, Paola, Adams, Douglas H., Blanco-Parra, Pilar & Díaz-Jaimes, Píndaro, 2025, Mitochondrial DNA patterns describe the evolutionary history of the bonnethead shark Sphyrna tiburo (Linneus 1758) complex in the western Atlantic Ocean, Journal of Fish Biology 106 (2), pp. 403-419 : 412-413

4.2 | Evolutionary history of the S. tiburo complex

The genetic differentiation of the S. tiburo complex, as evidenced by previous research and the present study, strongly suggests a divergence between the Northern (Carolina Province and the southern Gulf of Mexico) and Caribbean (which extended from Belize to Colombia) regions ( Fields et al., 2016; Gonzalez et al., 2019; Gonzalez et al., 2021). These two lineages coalesced between 3.9 and 4.8 MYA. This is concurrent with the timing of the full emergence of the CAI, which took place around 2.8–3.5 MYA ( Coates et al., 1992; Jaramillo, 2018; O'Dea et al., 2016). The emergence of the CAI caused profound changes in global ocean circulation, the evolution of tropical ecosystems, and potentially triggered the glaciation of the Northern Hemisphere ( Driscoll & Haug, 1998; Haug & Tiedemann, 1998). The reconstruction of ancestral areas indicated that the ancestors of the S. tiburo complex were distributed within the Northern region and subsequently dispersed southward into the Caribbean. Dispersal events may have occurred during the gradual shoaling of the Central American Seaway until 4.6 MYA when shoaling of the seaway reached <100 m on both sides of Panama and Costa Rica (Haug & Tiedemann, 1998). However, the closure was reaching completion only around 2.8–3.5 MYA ( Coates et al., 1992; Jaramillo, 2018; O'Dea et al., 2016). During that period, intensification of the Loop Current (Mullins et al., 1987), today a dominant feature of the ocean circulation that enters the Gulf of Mexico via the Yucatan Strait from the Caribbean Sea, may have isolated the S. tiburo complex through the Yucatan channel into the current two main clades: the Northern and Caribbean regions.

Subsequently, the divergence of the Northeastern Brazil lineage likely took place during the Pliocene and Pleistocene boundaries (1.6 and 2.5 MYA, respectively). The distribution of this lineage is closely associated with the Amazon-Orinoco Plume, which constitutes the largest volume of freshwater influx and sediment discharge in the world. It acts to modify local conditions, decreasing salinity (Pailler et al., 1999) and favoring turbid waters and fine terrigenous substrata due to the amount of sediment transported into the ocean (Leao & Dominguez, 2000). Particularly in this region, ecological differentiation has been suggested in a variety of reef fishes, but also in coastal sharks, such as the daggernose shark ( Carcharhinus oxyrhynchus ) and other elasmobranchs such as stingrays (subfamily: Potamotrygoninae) ( Fontenelle et al., 2021; Rocha et al., 2003, 2005; Rodrigues-Filho et al., 2023).

The Amazon-Orinoco Plume is a dynamic and complex system that began forming between 7 and 10 MYA (Hoorn et al., 2010). However, the sedimentation rate and freshwater discharge have fluctuated over time (Hoorn et al., 2017). The final formation period (about 2.4 MYA) was characterized by higher sedimentation and water discharge than in the initial development stages, but also marked by greater sea-level fluctuations, with high sea levels likely contributing to the passage of S. tiburo ancestors toward this biogeographic region. We hypothesized that a sufficient period of isolation would occur to subsequently drive evolutionary divergence. Alternatively, natural selection could also have played a role in the genetic differentiation of this lineage, ultimately enabling local adaptation (although this hypothesis should be evaluated with more variable nuclear markers). In this regard, the co-distributed coastal shark species, the daggernose shark ( C. oxyrhynchus ), exhibited morphological adaptations associated with murky environments (Rodrigues-Filho et al., 2023). Furthermore, differences in the head morphology and density of ampullae of Lorenzini have been detected between the Pacific and Caribbean clades of S. tiburo ( Aroca et al., 2022) . It is therefore likely that the Northeastern Brazil lineage could exhibit differences in the density of ampullae of Lorenzini as a potential result of enhanced feeding capacity in consistently turbid environments, as was recently observed in the daggernose shark (Haueisen & Reis, 2024). Morphological evaluation, together with an assessment of nuclear markers of the Northeastern Brazil lineage, is therefore essential to further evaluate this hypothesis.

More recently, the drop in sea level to 120 m during the last glacial maximum generated areas of exposed land masses that functioned as barriers to marine organisms ( Braconnot et al., 2007; O'Dea et al., 2016). Paleobathymetry models available from MARSPEC ( Braconnot et al., 2007) demonstrated the zones that could act as barriers to the movement of this species (Figure S3) and thus support the three genetic subdivisions found in this study. During glacial periods, the reduction in sea level may have interrupted the connectivity of suitable habitats and gene flow through the loss of suitable habitats and the formation of land barriers.

It is noteworthy that phylogeographic breaks analogous to those described here have been recorded in a variety of species, including other sharks, such as the smooth hammerhead ( S. zygaena ), scalloped hammerhead ( S. lewini ), night shark ( Carcharinus signatus [Poey, 1868]), silky shark ( Carcharinus falciformis [Müller & Henle, 1839]), bull shark ( Carcharinus leucas [Müller & Henle, 1839]), blacktip shark ( Carcharinus limbatus ), and lemon shark ( Negaprion brevirostris [Poey, 1868]) ( da Silva Ferrette et al., 2021; Dominguez, Hilsdorf, & Shivji et al. 2018; Domingues et al., 2019; Karl et al., 2011; Pinhal et al., 2020; Quattro et al., 2006; Schultz et al., 2008). This phenomenon has also been observed in other organisms, including reef fishes, sea anemones, prosobranch gastropods, and sea urchins of the genus Echinometra ( Giachini Tosetto et al., 2022; Mccartney et al., 2000; Rocha et al., 2008). This suggests that a biogeographic pattern consistent with the distinctions of the Northern, Caribbean, and Northeastern Brazil regions could be expected for many species, and aligns with the differences observed among biogeographic provinces. This pattern was even recorded in large hammerhead sharks that are distributed globally in pelagic habitats. Although these species have high migration capability, they remain dependent on coastal areas (e.g., for pupping and nursery habitats) where the geomorphology may restrict connectivity, leading to the genetic differentiation and spatial structuring associated with the biogeographic regions within the WA.