Ha. Lessios et al., Population structure and speciation in tropical seas: Global phylogeography of the sea urchin Diadema, EVOLUTION, 55(5), 2001, pp. 955-975
The causes of speciation in the sea are rarely obvious, because geographica
l barriers are not conspicuous and dispersal abilities or marine organisms,
particularly those of species with planktonic larvae, are hard to determin
e. The phylogenetic relations of species in cosmopolitan genera can provide
information on the likely mode of their formation. We reconstructed the ph
ylogeny of the pantropical and subtropical sea urchin genus Diadema, using
sequences of mitochondrial DNA from 482 individuals collected around the wo
rld, to determine the efficacy of barriers to gene flow and to ascertain th
e history of possible dispersal and vicariance events that led to speciatio
n. We also compared 22 isozyme loci between all described species except D.
palmeri. The mitochondrial DNA data show that the two deepest lineages are
found in the Indian and West Pacific Oceans. (Indo-Pacific) Diadema setosu
m diverged first from all other extant Diadema, probably during the initiat
ion of wide fluctuations in global sea levels in the Miocene. The D. setosu
m clade then split 3-5 million years ago into two clades, one found around
the Arabian Peninsula and the other in the Indo-West. Pacific. On the linea
ge leading to the other species of Diadema, the deepest branch is composed
of D. palmeri. apparently separated when the climate of New Zealand became
colder and other tropical echinoids at these islands went extinct. The next
lineage to separate is composed of a currently unrecognized species of Dia
dema that is found at Japan and the Marshall Islands. Diadema mexicanum in
the eastern Pacific separated next, whereas D. paucispinum. D. savignyi, an
d D. antillarum from the western and central Atlantic, and (as a separate c
lade) D. antillarum from the eastern Atlantic form a shallow polytomy. Appa
rently, Indo-Pacific populations of Diadema maintained genetic contact with
Atlantic ones around the southern tip of Africa for some time after the Is
thmus of Panama was complete. Diadema paucispinum contains two lineages: D.
paucispinum sensu stricto is not limited to Hawaii as previously thought,
but extends to Easter Island, Pitcairn, and Okinawa; A second mitochondrial
clade of D. paucispinum extends from East Africa and Arabia to the Philipp
ines and New Guinea. A more recent separation between West Indian Ocean and
West Pacific populations was detected in D. setosum. Presumably, these gen
etic discontinuities are the result of water flow restrictions in the strai
ts between northern Australia and Southeast Asia during Pleistocene episode
s of low sea level. Diadema savignyi is characterized by high rates of gene
how from Kiribati in the central Pacific all the way to the East African C
oast. In the Atlantic, there is a biogeographic barrier between the Caribbe
an and Brazil, possibly caused by fresh water outflow from the Amazon and t
he Orinoco Rivers. Diadema antillarum populations of the central Atlantic i
slands of Ascension and St. Helena are genetically isolated and phylogeneti
cally derived from Brazil. Except for its genetic separation by the mid-atl
antic barrier, Diadema seems to have maintained connections through potenti
al barriers to dispersal (including the Isthmus of Panama) more recently th
an did Eucidaris or Echinometra, two other genera of sea urchins in which p
hylogeography has been studied. Nevertheless, the mtDNA phylogeography of D
iadema includes all stages expected from models of allopatric differentiati
on.
There are anciently separated clades that now overlap in their geographic d
istribution, clades isolated in the periphery of the genus range that have
remained in the periphery, clades that may have been isolated in the periph
ery but have since spread towards the center, closely related clades on eit
her side of an existing barrier, and closely related monophyletic entities
on either side of an historical barrier that have crossed the former barrie
r line, but have not attained genetic equilibrium. Except for D. paucispinu
m and D. savignyi, in which known hybridization may have lodged mtDNA from
one species into the genome of the other, closely related clades are always
allopatric, and only distantly related ones overlap geographically. Thus,
the phylogenetic history and distribution of extant species of Diadema is b
y and large consistent with allopatric speciation.