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Historical dispersal of white sharks C. Gubili et al. 1683

of white sharks, catch data indicating movement into the Atlantic and Pacific, whereas the global population
cooler northern areas (the Adriatic) from the south (Tuni- is composed of clades specific to ocean basins. There is
sia and Sicilian Channel) in summer months. Consistent no recorded co-occurrence of clades in the Atlantic, as
with this, high summer sea surface temperature (SST) of is often cited for other pelagic species whose analogous
approximately 268C (close to the species’s upper limit phylogeographic patterns are explained by protracted uni-
[42]) in the Red Sea and adjacent waters, and a lack of directional gene flow from the Indo-Pacific into the
confirmed sightings, suggests this area acts as a thermal Atlantic [47]. Nor is there evidence of Pacific lineages
barrier, making a Lessepsian migration route less likely. in the southern Atlantic, which would also support such
So, what mechanism can be invoked to explain the a scenario. Additionally, palaeoclimatic reconstructions
anomalous presence of these haplotypes? Consideration of Pleistocene Atlantic SST [48] do not support retreat
of when the Mediterranean and Indo-Pacific sequences from the Atlantic to leave a relictual Mediterranean popu-
diverged may help elucidate this issue. lation during glacial maxima; temperatures remained
The lower estimate for white shark control region above the critical 158C threshold for white shark
mutation rate is similar to that of scalloped hammerheads movements in the Atlantic [49].
(0.8% [43]) and lemon sharks (0.67% [35]), corroborat- It would therefore seem a less than parsimonious
ing the slow evolution of elasmobranchs [44]. Hence, explanation to consider the GWS Pacific stock once ubi-
the MED/Indo-Pacific separation is estimated to have quitous but eradicated from the Atlantic during glacial
occurred in the Late Pleistocene (approx. 0.45 Ma), maxima. Conversely, glacial conditions promoting south-
roughly corresponding with the postulated origin of the ward expansion of Arctic fauna may have sustained rather
NEP population [19] (with the caveat that calculations than displaced white sharks in the equatorial Atlantic.
are based upon a single, unconserved region). Signifi- Rather, assuming that in situ divergence corresponds
cantly, the dynamic eustatic and climatic changes of this to an inter-glacial around Marine Isotope Stages 12
period have been implicated in promoting dramatic to 10, we suggest the estimated divergence time of
changes in population dynamics and range fluctuations Mediterranean and Pacific haplotypes at around
[45]. A recognized yet infrequent historical connection 450 Kya. Hence, historical accident during dramatic
between the Indo-Pacific, southwest Atlantic [46] and and dynamic Pleistocene climate change can be invoked
ultimately the Mediterranean open intermittently at this to explain Mediterranean white shark origins, at least par-
time has been used to explain the distribution of other tially. This scenario would be consistent with dominance
pelagic fish stocks [47]. This alternative longer route of few unique Pacific lineage haplotypes across the eastern
evokes eustatic regression events, widely accepted to pro- Mediterranean. A later migratory event following MED/
duce vicariance in pelagic species, entailing historical Indo-Pacific divergence cannot be ruled out, but could
dispersal across the Indian Ocean to South Africa, into be invoked by the same climatic trigger occurring
the Atlantic and north to the Straits of Gibraltar. Glacial repeatedly in the late Pleistocene.
events over the last 700 000 years have caused repeated The climatic instability of the Pleistocene may have
sea level falls of more than 80 m below present heights. induced navigational errors, with sharks following an
Notably, on such occasions the Sunda and Sahul shelves Agulhas ring or eddy. During inter-glacials of the last
formed a barrier between the Pacific and Indian Oceans, 700 000 years this would have been remarkably stronger
with vigorous leakage of Indian Ocean fauna later than the contemporary phenomenon [46], directing
facilitated by an enhanced Agulhas current during animals north along the African coast. Following expand-
Pleistocene inter-glacials [46]. This oceanic interchange ing swordfish and bluefin tuna populations, which arrived
has been suggested to account for the distribution of via these anomalous currents, a propensity to swim east to
Pacific clades of swordfish in the eastern Atlantic and natal grounds would have led ultimately to entrapment
particularly the Mediterranean, which they entered in the Mediterranean. Entrapment is also proposed
during an inter-glacial, surviving the last glacial maximum to account for the strong Indo-Pacific monophyletic mito-
(LGM) in an eastern refuge [47]. It could be argued chondrial signature of Mediterranean swordfish [47].
that swordfish and white sharks exhibit ecological com- Dominance of few distinct haplotypes over such a wide
monalities in their colonization of the Mediterranean. area would be wholly consistent with isolation, population
Both have similar temperature tolerances and natal philo- reduction, natal philopatry and restriction to eastern
patry [3,18], and swordfish are also prey of white sharks. Mediterranean refugia during glacial advances. Even if
However, though Alvarado-Bremer et al.[47] suggest that white sharks were able to penetrate the cooler Atlantic
some Mediterranean swordfish haplotypes are of Pacific at this time, natal philopatry, as evidenced by our juvenile
origin, they emphasize that the ubiquity and contempor- samples, would invariably associate these haplotypes
ary presence of these haplotypes in the southern with the Mediterranean. Genetic differences are also
Atlantic is consistent with sustained unidirectional gene apparent between northern Atlantic and Mediterranean
flow. Furthermore, despite evidence that the Mediterra- populations of other transoceanic dispersing marine pre-
nean stock survived the LGM isolated in the eastern dators, such as the sperm whale, Physeter macrocephalus
Mediterranean, their relationship with Pacific haplotypes [5]. Their differentiation can be explained by female
in the Atlantic suggests that glacial conditions did not philopatry, but their colonization is clearly attributable
erase the earlier signature of persistent migration into to a founder event involving northern Atlantic individ-
the Atlantic and subsequently the Mediterranean. uals. Like Lessepsian migrants, founding white sharks
Although several alternative hypotheses can be invoked may have encountered oceanographic characteristics and
to explain white shark colonization of the Mediterranean, prey availability in the eastern (as distinct from the
every scenario except historical infrequent long-distance western) Mediterranean basin approximating their Indo-
dispersal relies upon evidence of ubiquitous clades in Pacific natal areas. This scenario, consistent with the
Proc. R. Soc. B (2011)