Research ArticlePALEONTOLOGY

Exceptional preservation of mid-Cretaceous marine arthropods and the evolution of novel forms via heterochrony

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Science Advances  24 Apr 2019:
Vol. 5, no. 4, eaav3875
DOI: 10.1126/sciadv.aav3875
  • Fig. 1 Ventral and appendicular features in Callichimaera perplexa n. gen. n. sp., from the mid-Cretaceous of Colombia.

    (A to C) Holotype IGM p881215. (A) Ventral view. (B) Close-up of sternal plates, sutures, and linea media (lm); the white arrow shows a spine in the third leg coxae. (C) Close-up of sternal crown, mandibles, and maxillipeds 2 and 3, the latter bearing a row of spines or crista dentata (cd) in the ischium. (D and E) Paratype IGM p881196. (D) Ventral view. (E) Close-up of sternum and sutures. (F) Paratype IGM p881185, showing details of the spanner-like claw. (G to I) Paratype IGM p881214. (G) Close-up of the large oar-like legs 2 and 3. (H) Ventral view showing the sternites, claws, legs, and pleon. (I) Close-up of the reduced and slender legs 4 and 5. Ba, basis; Ca, carpus; Da, dactylus; Pr, propodus; Ma, mandibula; Me, merus; Mxp2 and Mxp3, second and third maxillipeds, respectively; P1, claw or cheliped; P2 to P5, pereopods or legs 2 to 5; Po, pollex or fixed finger tip; Pl, pleon or “abdomen”; S1 to S7, sternites 1 to 7; 4/5–6/7, sternal sutures. All specimens were photographed dry; specimens in (A), (D), (E), (G), and (H) were coated with ammonium chloride; specimens in (B), (C), (F), and (I) were uncoated. Photos by J.L.

  • Fig. 2 Dorsal, frontal, and ocular features in Callichimaera perplexa n. gen. n. sp., from the mid-Cretaceous of Colombia.

    (A and B) Paratype MUN-STRI 27044-02, showing three specimens in dorsal view (left), ventral view (right), and an isolated dorsal carapace (bottom center). (A) Color image. (B) Inverted color image highlighting details of the carapace outlines, claws and legs, and large eyes. (C) Paratype IMG p881203, dorsal view, showing details of the carapace grooves and ridges and the lack of true orbits. (D) Paratype IMG p881218, dorsal view, showing details of dorsal carapace, claws, and large oar-like legs 2 and 3. (E and F) Paratype IGM p881209a. (E) Scanning electron microscope (SEM) image showing details of large compound eye, optical lobe, rostrum (R), and two pairs of short antennae between the eyes. (F) SEM showing a close-up of the optical lobe. (G) Paratype IGM p881220, SEM of large eye preserving mostly hexagonal facets in hexagonal arrangement (left box), although the proximal cornea bears squarish facets in orthogonal packing (right box). (H to J) Paratype IGM p881208, ventral view, (H) showing the large eyes and bifid rostrum, (I) SEM of ventral right eye, and (J) SEM of ventral left eye. An1, antenna 1 or antennula; An2, antenna 2; Bcg, branchio-cardiac groove; Cg, cervical groove; E, compound eye; Lr, longitudinal ridge; Ol, optical lobe; Pfr, postfrontal longitudinal ridge; Pgr, protogastric longitudinal ridge. All specimens were photographed dry; specimens in (C) and (D) were coated with ammonium chloride; specimens in (A), (B), and (E) to (J) were uncoated. Photos by J.L.

  • Fig. 3 Pleon and sexual dimorphism in Callichimaera perplexa n. gen. n. sp., lower Upper Cretaceous, Colombia.

    (A) Paratype IMG p881217, female, dorsal view showing the legs 2 to 5 and the pleonites 1 to 4, two of them bearing an axial tubercle. (B) Paratype IGM p881209b, female, showing the unfolded pleon in lateral view and pleonites 2 to 5 and multiple pairs of pleopods (white arrows). (C) Paratype MUN-STRI 27045-06, female, dorsal view, showing pleonites 1 to 6, the roundish telson, and the lack of uropods or uropodal plates. (D and E) Paratype IGM p881202, male. (D) Ventral view showing the chelipeds, pereopods, and pleon with sclerotized gonopods 1 and 2 [white box; see (E)]. (E) Close-up of sclerotized male gonopods 1 and 2 (white arrows), a narrow pleonite 6, an elongate telson, and the lack of uropods or uropodal plates. (F) Line drawing of (E). (G) Paratype MUN-STRI 27045-09, a very small individual, possibly a megalopa or early postlarval stage, preserving small and slender legs 2 and 3 compared to adult forms [see (I)]. (H) Paratype IGM p881220, juvenile, with legs 2 and 3, the pleon bearing an axial tubercle, and with a bifid rostrum and a pair of large compound eyes bearing hexagonal facets (Fig. 2G). (I) Paratype IGM p881206, adult female, ventral view preserving spanner-like chelipeds, long oar-like legs or P2 and P3, reduced and slender legs or P4 and P5, and a broad pleon. G1 and G2, male gonopods 1 and 2; Pl1 to Pl6, pleonites 1 to 6; T, telson. All specimens were photographed dry; specimens in (A), (C), (D), and (G) to (I) were coated with ammonium chloride; specimens in (B) and (E) were uncoated. Photos by J.L.

  • Fig. 4 Callichimaera perplexa n. gen. n. sp., reconstruction.

    (A and B) Line drawing of dorsal (A) and ventral (B) views. Colors denote convergent traits with other decapod groups: light gray, dorsal carapace, similar to some lobsters and †Palaeocorystidae (Brachyura: Raninoida); dark gray, large eyes, similar to †Ekalakia (Dromiacea: †Glaessneropsidae) and several homoloids; red, pediform mxp3 bearing a crista dentata, similar to lobsters, most anomurans, and early-branching brachyurans (Homolodromioidea, most Homoloidea); yellow, spanner-like P1, similar to Hippoidea (Anomura), Raninoidea (Brachyura), and †Retrorsichela; green, flattened paddle-like legs P2 and P3, similar to Matutidae (Brachyura: Eubrachyura); blue, reduced legs P4 and P5, as in hermit crabs (Anomura: Paguroidea), podotreme brachyurans (e.g., Homolodromioidea and Cyclodorippoidea) and early-branching eubrachyurans (e.g., Dorippoidea); orange, sternites S5 and S6 similar to †Retrorsichela, and Heikeopsis (Eubrachyura: Dorippoidea); and purple, symmetrical pleon lacks articulated rings and uropods/uropodal plates, like most brachyurans. (C and D) Digital reconstruction. (C) Dorsal view. (D) Ventral view. A, pleon; Cx, coxa; Is, ischium; Ma, manus. Scale bar, 10 mm. See movies S1 and S2 and data file S2 for three-dimensional (3D) viewable and printable models. Line drawings by J.L. and 3D reconstructions by A.D.

  • Fig. 5 Phylogenetic relationships among the main families, superfamilies, and sections of “true” crabs or Brachyura.

    Tree topology after figs. S5 and S6. Each color and letter (encircled) represents one of the nine major brachyuran evolutionary branches. Dromiacea (red) (A) and Homoloida (purple) (B) are first known from the Jurassic, while †Callichimaeroida section nov. (dark blue) (C), †Torynommoida (light blue) (D), †Etyoida (dark green) (E), Raninoida (light green) (F), †Dakoticancroida (yellow) (G), Cyclodorippoida (orange) (H), and Eubrachyura or “higher” brachyurans (brown) (I) are all first known from the Cretaceous. Thick solid lines represent the ages of the first and last occurrences of each family within the main lineages. Dotted lines and daggers indicate extinct taxa; solid lines indicate living taxa. Black triangles indicate that in Anomura, decarcinization has occurred twice (anomuran clades not illustrated). White triangles indicate the three Brachyura lineages where decarcinization has occurred. Figure by J.L.

  • Fig. 6 Convergent decarcinized body forms in various families of false and true crabs and convergent appendages in swimming and/or fossorial arthropods.

    (A to I) Decarcinized crabs. (A to D) Anomura. (A to C) Mole crabs, Hippoidea: (A) Hippidae, Hippa marmorata, Taiwan. (B) Blepharipodidae: Blepharipoda occidentalis. (C) Albuneidae: Albunea occulta, Taiwan.. (D) Porcelain crabs, Galatheoidea: Porcellanidae: Euceramus panatelus, Panama. (E to I) Brachyura. (E and F) Frog crabs, Raninoidea: Raninidae: (E) Raninoides benedicti, Panamá. (F) Symethis sp. Panamá. (G and H) Masked burrowing crabs, Eubrachyura: Corystoidea: Corystidae: (G) Corystes cassivelaunus, Belgium. (H) Jonas distinctus, Taiwan. (I) Chimera crab, †Callichimaeroidea: Callichimaeridae: Callichimaera perplexa n. gen. n. sp., Cenomanian-Turonian (95 to 90 Ma ago) of Colombia. (J to Q) Other aquatic arthropods with modified appendages for swimming and/or digging. (J) Sea scorpions, Chelicerata: †Eurypterida: Eurypterus remipes, YPM 211521, upper Silurian, New York. (K to M) Insecta. (K) Coleoptera: Dytiscidae: Cybister fimbriolatus, YPM ENT.959234; (L) Hemiptera: Corixidae: Hesperocorixa kennicottii, YPM ENT.452851; (M) Hemiptera: Notonectidae: Notonecta undulate, last instar nymph, Alberta, Canada. (N) Isopoda: Munnopsidae: Munnopsis longiremis, USNM 113282, Baja California, Mexico. (O to Q) Brachyura. (O) Orithyioidea: Orithyiidae: Orithyia sinica, USNM 134243, China. (P) Calappoidea: Matutidae: Matuta victor. (Q) Portunoidea: Portunidae: Arenaeus cribrarius. Photos by T. Y. Chan (A, C, and H), C. Boyko (B), A. Anker (D, E, and N), J.L. (F and O), H. Hillewaert (G), J. Utrup (J), E. Lazo-Wasem (K and L), J. Acorn (M), and O. Radosta (P and Q).

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/5/4/eaav3875/DC1

    Supplementary Text

    Fig. S1. Paleogeographic map during early Late Cretaceous times (~95 to 90 Ma ago).

    Fig. S2. Stratigraphic column of the Cenomanian-Turonian Churuvita Group in the studied area.

    Fig. S3. Crustacean-dominated faunule at the studied section.

    Fig. S4. Additional dorsal, ventral, and appendicular features in Callichimaera perplexa n. gen. n. sp., from the mid-Cretaceous of Colombia and the United States.

    Fig. S5. MP-strict consensus of a single most parsimonious tree for the nine major brachyuran sections and podotreme brachyuran families, including Callichimaeridae n. fam.

    Fig. S6. Results of equally weighted and IWMP analyses.

    Fig. S7. ML topology with the nine major brachyuran sections and podotremous brachyuran families, including Callichimaeridae n. fam.

    Fig. S8. Bayesian majority-rule consensus topology of the post-burnin sample of trees for fossil and extant podotremous brachyuran families, including Callichimaeridae n. fam.

    Table S1. List of characters for phylogenetic analysis.

    Table S2. Superfamilies and families of anomuran and brachyuran crabs included in the phylogenetic analysis.

    Data file S1. Data matrix for phylogenetic analysis.

    Data file S2. Printable 3D model file of Callichimaera perplexa n. gen. n. sp.

    Movie S1. Dorsoventral view 3D reconstruction of Callichimaera perplexa n. gen. n. sp.

    Movie S2. Side view 3D reconstruction of Callichimaera perplexa n. gen. n. sp.

    References (80146)

  • Supplementary Materials

    The PDF file includes:

    • Supplementary Text
    • Fig. S1. Paleogeographic map during early Late Cretaceous times (~95 to 90 Ma ago).
    • Fig. S2. Stratigraphic column of the Cenomanian-Turonian Churuvita Group in the studied area.
    • Fig. S3. Crustacean-dominated faunule at the studied section.
    • Fig. S4. Additional dorsal, ventral, and appendicular features in Callichimaera perplexa n. gen. n. sp., from the mid-Cretaceous of Colombia and the United States.
    • Fig. S5. MP-strict consensus of a single most parsimonious tree for the nine major brachyuran sections and podotreme brachyuran families, including Callichimaeridae n. fam.
    • Fig. S6. Results of equally weighted and IWMP analyses.
    • Fig. S7. ML topology with the nine major brachyuran sections and podotremous brachyuran families, including Callichimaeridae n. fam.
    • Fig. S8. Bayesian majority-rule consensus topology of the post-burnin sample of trees for fossil and extant podotremous brachyuran families, including Callichimaeridae n. fam.
    • Table S1. List of characters for phylogenetic analysis.
    • Table S2. Superfamilies and families of anomuran and brachyuran crabs included in the phylogenetic analysis.
    • References (80146)

    Download PDF

    Other Supplementary Material for this manuscript includes the following:

    • Data file S1 (.nex format). Data matrix for phylogenetic analysis.
    • Data file S2 (.obj format). Printable 3D model file of Callichimaera perplexa n. gen. n. sp.
    • Movie S1 (.mp4 format). Dorsoventral view 3D reconstruction of Callichimaera perplexa n. gen. n. sp.
    • Movie S2 (.mp4 format). Side view 3D reconstruction of Callichimaera perplexa n. gen. n. sp.

    Files in this Data Supplement:

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