Figure 1.
Geographical pattern of distribution of the Clupeoidei.
A) Distribution and species diversity of Clupeoidei. Number of species per grid cell (4 by 4 degree latitude-longitude resolution) is represented by cool (low diversity) to warm (high diversity) colors. Individual species distribution compiled from Whitehead [16] and Whitehead et al. [17], Wongratana [125], Gourène and Teugels [126], Peng and Zhao [127], Castro-Aguirre and Viverro [128], Randall [129], Nelson and McCarthy [130], Siebert [34], Britz and Kottelat [131], Menezes and De Pinna [132], Stiassny [97], Castro-Aguirre et al. [133], Roberts [134], Borsa et al. [135], Kimura et al. [136], Loeb [13], DiBattista et al. [14] and Randall and DiBattista [137]. B) The 12 biogeographical units used in the ancestral ranges reconstruction analysis; each unit was delimited by landmasses, vast expanses of open ocean and water temperature. Within each region, total number of clupeoid species (in regular) and number of endemics (in bold) are indicated in parentheses.
Figure 2.
Maximum likelihood tree of the Clupeoidei from analysis of the mitogenomic dataset (using RAxML [99]).
Branch lengths are proportional to the number of substitutions per nucleotide position (scale bar = 0.05 substitutions). Numbers at nodes are Bootstrap proportions (in percentage). The tree is rooted with Coregonus lavaretus and Esox lucius. Abbreviation: C., Chirocentrus.
Figure 3.
Phylogenetic chronogram of the Clupeoidei based on a Bayesian relaxed clock analysis (using BEAST v1.7.4 [103]) of the mitogenomic dataset, calibrated with seven fossil-based constraints (see text for details).
Coregonus lavaretus and Esox lucius are together used to root the tree. Horizontal timescale is in million years before present (Mya) (Paleogene Epoch abbreviations: Paleo, Paleocene; Eo, Eocene; and Oligo, Oligocene). Black horizontal bars (indicating calibration constraints on the corresponding nodes) and light grey gradient horizontal bars at nodes are 95% age credibility intervals. Numbers given at nodes are the Bayesian posterior probabilities when <1. Black arrowheads indicate the crown group origins of lineages of Clupeoidei as discussed in the text.
Figure 4.
Reconstructions of the evolution of salinity and water temperature preference within the Clupeoidei using likelihood optimization on the Bayesian time-tree topology (see Fig. 3).
A) Salinity preference classified in three states: “marine” indicated in white, “euryhaline” in black, and “freshwater” in green. At each node, the relative probabilities of each state (sum = 1) are drawn using pie charts. Black arrowheads indicate transition from marine to euryhaline or freshwater environments. B) Water temperature preference classified in two states: “tropical” indicated in white and “temperate” in black. At each node, the relative probabilities of each state (sum = 1) are drawn using pie charts. Black arrowheads indicate transition from tropical to temperate environments.
Figure 5.
Most likely ancestral ranges reconstruction of the Clupeoidei during the Cretaceous and early Cenozoic period using the dispersal–extinction–cladogenesis (DEC) model [116], [117] onto a simplified Bayesian phylogenetic chronogram.
Outgroups (i.e., non-clupeoids) were deleted and biogeographically redundant clupeoid taxa were merged with their respective sister group (see material and methods for details). Ancestral ranges at nodes within each major lineage not reconstructed. Horizontal timescale in million of years ago (Mya) (Paleogene epoch abbreviations: Paleo, Paleocene; Eo, Eocene; and Oligo, Oligocene). Most likely ancestral ranges reconstruction at nodes indicated by code-color boxes (see Fig. 1B for correspondence between regions and two or three-letter codes and colors). Black arrows indicate the three dispersal events predating or likely predating the K-Pg boundary and black arrowheads indicate subsequent allopatric cladogenesis. Temperate lineage branches are underlined in blue and white arrowheads indicate marine to freshwater transitions. “*” after a species name indicates that closely related species to this species have been pruned (see material and methods for details); “**” after a species name indicates that this species is a representative of a supra-specific group having a larger geographical distribution. “NC” at nodes indicate that the ancestral ranges were not estimated at these nodes. On the left side, the spatio-temporal context is illustrated with four schematic paleoreconstructions (at 90, 65 and 50 Mya) on which are indicated the temporally corresponding clupeoid fossil localities by white (marine/brackish) and grey (freshwater) stars. Emerged lands are displayed in black and marine environments in blue with the shallow parts in lighter blue. One additional reconstruction (D) shows the current geographical context with the biogeographical units. The clupeoid fossil localities are: 1- the Cenomanian locality “Loma la Mula” in Coahuila, northeastern Mexico (taxon:†Scombroclupea occidentalis currently considered as a clupeid incertae sedis) [88]; 2- the marine shale yielded in the Taquari Member (Albian) of Riachuelo Formation (state of Sergipe, Northeastern Brazil) (taxon:†Nolfia riachuelensis currently considered as a clupeid ad interim) [81]; 3- the marine deposit from the Cenomanian of Kipala, Democratic Republic of Congo (taxon:†Nolfia kwangoensis currently considered as a clupeid incertae sedis) and the marine Santonian of Vonso, Democratic Republic of Congo (taxon:†Audenaerdia casieri currently considered as a clupeid incertae sedis) [85], [89]; 4- the Cenomanian (Upper Cretaceous) Komen (Slovenia) fossil lagerstätte (taxon: †Scombroclupea macrophthalma currently considered as a clupeoid incertae sedis); [83], [138]; 5- the Cenomanian fossil fish localities of Lebanon (e.g., Namoura, Hakel and Hajula) (taxa: †Scombroclupea spp. currently considered as clupeoids incertae sedis) [83]; 6- the Upper Cretaceous (Maastrichtian) of Cayara, El Molino Formation, Bolivia (taxon:†Gastroclupea branisai currently considered as a pristigasterid incertae sedis) [39], [81]; 7- the Upper Cretaceous (Campano-Maastrichtian limit, 74.0 Mya) marine sediments of Nardò, Italy (taxa: †Portoselvaggioclupea whiteheadi and †Nardoclupea grandei [Dussumieriinae], †Pugliaclupea nolardi [Clupeinae], †Lecceclupea ehiravaensis [Pellonulinae], and †Italoclupea nolfi [Alosinae]) [51]–[54]; 8- The Middle Paleocene Tongue River Formation (lacustrine limestone), near Bay Horse, Montana, USA (taxon: †Knightia vetusta currently considered as a clupeoid incertae sedis) [40]; 9- the Middle Eocene Laney Member of the Green River Formation, southwestern Wyoming, USA (lacustrine deposits)(taxon: †Gosiutichthys parvus currently considered as a clupeoid incertae sedis) and the Lower Eocene lacustrine sediments of Wyoming, Colorado and Utah, USA (taxa: †Knightia alta and †Knightia eocaena currently considered as clupeoids incertae sedis) [40]; 10- the Lower Eocene (52.0 Mya) marine sediments of Monte Bolca, Italy (taxa: several species of Clupeidae including at least one species of Dussumieriinae sensu Grande [18]); 11- the Upper Paleocene freshwater lacustrine deposits of Bamanbor and Ninania of Saurashtra, India (taxon: †Horaclupea intertrappea currently considered as a clupeid incertae sedis) and the Eocene Saline Series of the Salt range of Pakistan (taxon: the clupeid †Horaclupea geei) [18]; 12- the Late Paleocene fish fauna of the Danata Formation in Turkmenistan (taxon: †Primisardinella genetrix currently considered as a clupeid incertae sedis) [18] and 13- the Eocene (probably freshwater) deposits of Hupei, China (taxon: †Knightia yuyanga currently considered as a clupeid incertae sedis) [18].