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Life habits, hox genes, and affinities of a 311 million-year-old holometabolan larva.

Haug JT, Labandeira CC, Santiago-Blay JA, Haug C, Brown S - BMC Evol. Biol. (2015)

Bottom Line: Srokalarva berthei occurred in an evolutionary developmental context likely responsible for the early macroevolutionary success of holometabolous insects.Srokalarva berthei body features suggest a caterpillar-like body plan and head structures indicating herbivory consistent with known, contemporaneous insect feeding damage on seed plants.Taxonomic resolution places Srokalarva berthei as an extinct lineage, apparently possessing features closer to neuropteroid than other holometabolous lineages.

View Article: PubMed Central - PubMed

Affiliation: Ludwig Maximilians University Munich, Biocenter - Department of Biology II and GeoBio-Center, Großhaderner Str. 2, Planegg-Martinsried, 82152, Germany.

ABSTRACT

Background: Holometabolous insects are the most diverse, speciose and ubiquitous group of multicellular organisms in terrestrial and freshwater ecosystems. The enormous evolutionary and ecological success of Holometabola has been attributed to their unique postembryonic life phases in which nonreproductive and wingless larvae differ significantly in morphology and life habits from their reproductive and mostly winged adults, separated by a resting stage, the pupa. Little is known of the evolutionary developmental mechanisms that produced the holometabolous larval condition and their Paleozoic origin based on fossils and phylogeny.

Results: We provide a detailed anatomic description of a 311 million-year-old specimen, the oldest known holometabolous larva, from the Mazon Creek deposits of Illinois, U.S.A. The head is ovoidal, downwardly oriented, broadly attached to the anterior thorax, and bears possible simple eyes and antennae with insertions encircled by molting sutures; other sutures are present but often indistinct. Mouthparts are generalized, consisting of five recognizable segments: a clypeo-labral complex, mandibles, possible hypopharynx, a maxilla bearing indistinct palp-like appendages, and labium. Distinctive mandibles are robust, triangular, and dicondylic. The thorax is delineated into three, nonoverlapping regions of distinctive surface texture, each with legs of seven elements, the terminal-most bearing paired claws. The abdomen has ten segments deployed in register with overlapping tergites; the penultimate segment bears a paired, cercus-like structure. The anterior eight segments bear clawless leglets more diminutive than the thoracic legs in length and cross-sectional diameter, and inserted more ventrolaterally than ventrally on the abdominal sidewall.

Conclusions: Srokalarva berthei occurred in an evolutionary developmental context likely responsible for the early macroevolutionary success of holometabolous insects. Srokalarva berthei bore head and prothoracic structures, leglet series on successive abdominal segments - in addition to comparable features on a second taxon eight million-years-younger - that indicates Hox-gene regulation of segmental and appendage patterning among earliest Holometabola. Srokalarva berthei body features suggest a caterpillar-like body plan and head structures indicating herbivory consistent with known, contemporaneous insect feeding damage on seed plants. Taxonomic resolution places Srokalarva berthei as an extinct lineage, apparently possessing features closer to neuropteroid than other holometabolous lineages.

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Thoracic and abdominal appendages of Srokalarva berthei. a to d, Second (mesothoracic) and third (metathoracic) appendages; (e) to (g), True first abdominal appendage. a, e, Directed low angle light. b, Undirected reflected light. Arrows mark patterns resembling supposed claw. c, Red-blue anaglyph of a virtual surface reconstruction. (Use red-cyan glasses to view.) d, Interpretative version of (c). f, Red-cyan stereo-anaglyph under cross-polarized light. (Use red-cyan glasses to view.) g, Interpretative version of (f). Abbreviations: “cl”, originally interpreted claw; tr, tergite rim
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Fig3: Thoracic and abdominal appendages of Srokalarva berthei. a to d, Second (mesothoracic) and third (metathoracic) appendages; (e) to (g), True first abdominal appendage. a, e, Directed low angle light. b, Undirected reflected light. Arrows mark patterns resembling supposed claw. c, Red-blue anaglyph of a virtual surface reconstruction. (Use red-cyan glasses to view.) d, Interpretative version of (c). f, Red-cyan stereo-anaglyph under cross-polarized light. (Use red-cyan glasses to view.) g, Interpretative version of (f). Abbreviations: “cl”, originally interpreted claw; tr, tergite rim

Mentions: The thoracic segments do not differ markedly from the abdominal segments in the original interpretation. Our observations contradict this view. Three, well-delineated, nonoverlapping and noninterlinking regions of thoracic sclerites are apparent from an assessment of surface relief and color (Fig. 1a, d; Additional file 1: Figure S1A,D). The three thoracic legs are significantly more robust, longer and possess a greater diameter than the abdominal leglets. Originally thoracic legs were reconstructed with seven elements, whereas we found five major elements with a possible sixth element bearing terminal paired claws that are variably preserved (Fig. 3a–d). Although dark lines occur on sclerite surfaces and were interpreted originally as setae [6], and Mazon Creek fossils occasionally preserve fine hairs [15], we found no evidence for hirsute integument. Areas between the sclerites appear to preserve softer cuticle. These observations indicate that the thorax extends further rearward than the original reconstruction, corresponding to the anterior five postcephalic segments of Kukalová-Peck [6], and is more differentiated from the abdomen than originally reconstructed. The abdominal segments are in register (body segments matching respective leglets), but with overlapping tergites, the exact intersegmental boundaries are difficult to discern. This is borne out by a lack of an exact match of tergites between part and counterpart.Fig. 3


Life habits, hox genes, and affinities of a 311 million-year-old holometabolan larva.

Haug JT, Labandeira CC, Santiago-Blay JA, Haug C, Brown S - BMC Evol. Biol. (2015)

Thoracic and abdominal appendages of Srokalarva berthei. a to d, Second (mesothoracic) and third (metathoracic) appendages; (e) to (g), True first abdominal appendage. a, e, Directed low angle light. b, Undirected reflected light. Arrows mark patterns resembling supposed claw. c, Red-blue anaglyph of a virtual surface reconstruction. (Use red-cyan glasses to view.) d, Interpretative version of (c). f, Red-cyan stereo-anaglyph under cross-polarized light. (Use red-cyan glasses to view.) g, Interpretative version of (f). Abbreviations: “cl”, originally interpreted claw; tr, tergite rim
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4587847&req=5

Fig3: Thoracic and abdominal appendages of Srokalarva berthei. a to d, Second (mesothoracic) and third (metathoracic) appendages; (e) to (g), True first abdominal appendage. a, e, Directed low angle light. b, Undirected reflected light. Arrows mark patterns resembling supposed claw. c, Red-blue anaglyph of a virtual surface reconstruction. (Use red-cyan glasses to view.) d, Interpretative version of (c). f, Red-cyan stereo-anaglyph under cross-polarized light. (Use red-cyan glasses to view.) g, Interpretative version of (f). Abbreviations: “cl”, originally interpreted claw; tr, tergite rim
Mentions: The thoracic segments do not differ markedly from the abdominal segments in the original interpretation. Our observations contradict this view. Three, well-delineated, nonoverlapping and noninterlinking regions of thoracic sclerites are apparent from an assessment of surface relief and color (Fig. 1a, d; Additional file 1: Figure S1A,D). The three thoracic legs are significantly more robust, longer and possess a greater diameter than the abdominal leglets. Originally thoracic legs were reconstructed with seven elements, whereas we found five major elements with a possible sixth element bearing terminal paired claws that are variably preserved (Fig. 3a–d). Although dark lines occur on sclerite surfaces and were interpreted originally as setae [6], and Mazon Creek fossils occasionally preserve fine hairs [15], we found no evidence for hirsute integument. Areas between the sclerites appear to preserve softer cuticle. These observations indicate that the thorax extends further rearward than the original reconstruction, corresponding to the anterior five postcephalic segments of Kukalová-Peck [6], and is more differentiated from the abdomen than originally reconstructed. The abdominal segments are in register (body segments matching respective leglets), but with overlapping tergites, the exact intersegmental boundaries are difficult to discern. This is borne out by a lack of an exact match of tergites between part and counterpart.Fig. 3

Bottom Line: Srokalarva berthei occurred in an evolutionary developmental context likely responsible for the early macroevolutionary success of holometabolous insects.Srokalarva berthei body features suggest a caterpillar-like body plan and head structures indicating herbivory consistent with known, contemporaneous insect feeding damage on seed plants.Taxonomic resolution places Srokalarva berthei as an extinct lineage, apparently possessing features closer to neuropteroid than other holometabolous lineages.

View Article: PubMed Central - PubMed

Affiliation: Ludwig Maximilians University Munich, Biocenter - Department of Biology II and GeoBio-Center, Großhaderner Str. 2, Planegg-Martinsried, 82152, Germany.

ABSTRACT

Background: Holometabolous insects are the most diverse, speciose and ubiquitous group of multicellular organisms in terrestrial and freshwater ecosystems. The enormous evolutionary and ecological success of Holometabola has been attributed to their unique postembryonic life phases in which nonreproductive and wingless larvae differ significantly in morphology and life habits from their reproductive and mostly winged adults, separated by a resting stage, the pupa. Little is known of the evolutionary developmental mechanisms that produced the holometabolous larval condition and their Paleozoic origin based on fossils and phylogeny.

Results: We provide a detailed anatomic description of a 311 million-year-old specimen, the oldest known holometabolous larva, from the Mazon Creek deposits of Illinois, U.S.A. The head is ovoidal, downwardly oriented, broadly attached to the anterior thorax, and bears possible simple eyes and antennae with insertions encircled by molting sutures; other sutures are present but often indistinct. Mouthparts are generalized, consisting of five recognizable segments: a clypeo-labral complex, mandibles, possible hypopharynx, a maxilla bearing indistinct palp-like appendages, and labium. Distinctive mandibles are robust, triangular, and dicondylic. The thorax is delineated into three, nonoverlapping regions of distinctive surface texture, each with legs of seven elements, the terminal-most bearing paired claws. The abdomen has ten segments deployed in register with overlapping tergites; the penultimate segment bears a paired, cercus-like structure. The anterior eight segments bear clawless leglets more diminutive than the thoracic legs in length and cross-sectional diameter, and inserted more ventrolaterally than ventrally on the abdominal sidewall.

Conclusions: Srokalarva berthei occurred in an evolutionary developmental context likely responsible for the early macroevolutionary success of holometabolous insects. Srokalarva berthei bore head and prothoracic structures, leglet series on successive abdominal segments - in addition to comparable features on a second taxon eight million-years-younger - that indicates Hox-gene regulation of segmental and appendage patterning among earliest Holometabola. Srokalarva berthei body features suggest a caterpillar-like body plan and head structures indicating herbivory consistent with known, contemporaneous insect feeding damage on seed plants. Taxonomic resolution places Srokalarva berthei as an extinct lineage, apparently possessing features closer to neuropteroid than other holometabolous lineages.

Show MeSH
Related in: MedlinePlus