Limits...
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.

Show MeSH

Related in: MedlinePlus

The external body structure of Srokalarva berthei. a and b are the part of specimen MCP-322; (c) and (d) are the counterpart to MCP-322, representing approximate mirror images of each other. a and d, Red–cyan stereo anaglyphs imaged under cross-polarized light. (For best visual results, use red–cyan glasses for viewing.) (b) and (c), Interpretative versions of (a) and (d), respectively. Colors delimit regions of the head, tergites, thoracic membranous regions, and appendages such as mouthparts, thoracic legs and abdominal prolegs. Arrows indicate abbreviated appendages on abdominal segment 9. Note that the proximal regions of the appendages are concealed under the body, and are not clearly marked. Abbreviations: aa, abdominal appendages; a1–a9, abdominal segments 1 to 9; hc, head capsule; ta, thoracic appendages; tt, trunk tergites
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig1: The external body structure of Srokalarva berthei. a and b are the part of specimen MCP-322; (c) and (d) are the counterpart to MCP-322, representing approximate mirror images of each other. a and d, Red–cyan stereo anaglyphs imaged under cross-polarized light. (For best visual results, use red–cyan glasses for viewing.) (b) and (c), Interpretative versions of (a) and (d), respectively. Colors delimit regions of the head, tergites, thoracic membranous regions, and appendages such as mouthparts, thoracic legs and abdominal prolegs. Arrows indicate abbreviated appendages on abdominal segment 9. Note that the proximal regions of the appendages are concealed under the body, and are not clearly marked. Abbreviations: aa, abdominal appendages; a1–a9, abdominal segments 1 to 9; hc, head capsule; ta, thoracic appendages; tt, trunk tergites

Mentions: Although holometabolous (endopterygote) insects are the pre-eminent macroscopic animals that structure terrestrial ecosystems today [1], very little is known of their late Paleozoic origins when life on land was overwhelmingly dominated by nonholometabolous insects and a myriad of other arthropod lineages [2]. Various proposals have been offered to explain the evolutionary transition from non-holometabolous to holometabolous in insects [2–4]. Although these evolutionary developmental mechanisms have been addressed by evidence from modern model organisms [3, 4], there is minimal data from the deep-time fossil record regarding the origin of this unique developmental innovation. The Paleozoic fossil record of holometabolous larvae is extremely sparse [6–8], particularly for the time interval during which crucial developments likely occurred [9, 10]. One recent discovery is a holometabolous larva from the Late Pennsylvanian Period of Germany, Metabolarva bella [8]. However, insufficient structural details are known about this larva and it remains unplaced in an evolutionary developmental context that would lend understanding of how holometaboly originated. The only other early fossil of a presumptive holometabolous larva is from the older Middle Pennsylvanian Period, Srokalarva berthei (Fig. 1, Additional file 1: Figures S1 and S2), an informal designation provided by Kukalová-Peck [6]. The holometabolous identity of the single specimen of Srokalarva berthei repeatedly has been questioned [11–13], but without examination of the fossil (see Additional file 1 for a taxonomic assessment). We present a detailed morphological description of Srokalarva berthei based on current imaging techniques (Additional file 1), and indicate its significance for early evolution of Holometabola.Fig. 1


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)

The external body structure of Srokalarva berthei. a and b are the part of specimen MCP-322; (c) and (d) are the counterpart to MCP-322, representing approximate mirror images of each other. a and d, Red–cyan stereo anaglyphs imaged under cross-polarized light. (For best visual results, use red–cyan glasses for viewing.) (b) and (c), Interpretative versions of (a) and (d), respectively. Colors delimit regions of the head, tergites, thoracic membranous regions, and appendages such as mouthparts, thoracic legs and abdominal prolegs. Arrows indicate abbreviated appendages on abdominal segment 9. Note that the proximal regions of the appendages are concealed under the body, and are not clearly marked. Abbreviations: aa, abdominal appendages; a1–a9, abdominal segments 1 to 9; hc, head capsule; ta, thoracic appendages; tt, trunk tergites
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig1: The external body structure of Srokalarva berthei. a and b are the part of specimen MCP-322; (c) and (d) are the counterpart to MCP-322, representing approximate mirror images of each other. a and d, Red–cyan stereo anaglyphs imaged under cross-polarized light. (For best visual results, use red–cyan glasses for viewing.) (b) and (c), Interpretative versions of (a) and (d), respectively. Colors delimit regions of the head, tergites, thoracic membranous regions, and appendages such as mouthparts, thoracic legs and abdominal prolegs. Arrows indicate abbreviated appendages on abdominal segment 9. Note that the proximal regions of the appendages are concealed under the body, and are not clearly marked. Abbreviations: aa, abdominal appendages; a1–a9, abdominal segments 1 to 9; hc, head capsule; ta, thoracic appendages; tt, trunk tergites
Mentions: Although holometabolous (endopterygote) insects are the pre-eminent macroscopic animals that structure terrestrial ecosystems today [1], very little is known of their late Paleozoic origins when life on land was overwhelmingly dominated by nonholometabolous insects and a myriad of other arthropod lineages [2]. Various proposals have been offered to explain the evolutionary transition from non-holometabolous to holometabolous in insects [2–4]. Although these evolutionary developmental mechanisms have been addressed by evidence from modern model organisms [3, 4], there is minimal data from the deep-time fossil record regarding the origin of this unique developmental innovation. The Paleozoic fossil record of holometabolous larvae is extremely sparse [6–8], particularly for the time interval during which crucial developments likely occurred [9, 10]. One recent discovery is a holometabolous larva from the Late Pennsylvanian Period of Germany, Metabolarva bella [8]. However, insufficient structural details are known about this larva and it remains unplaced in an evolutionary developmental context that would lend understanding of how holometaboly originated. The only other early fossil of a presumptive holometabolous larva is from the older Middle Pennsylvanian Period, Srokalarva berthei (Fig. 1, Additional file 1: Figures S1 and S2), an informal designation provided by Kukalová-Peck [6]. The holometabolous identity of the single specimen of Srokalarva berthei repeatedly has been questioned [11–13], but without examination of the fossil (see Additional file 1 for a taxonomic assessment). We present a detailed morphological description of Srokalarva berthei based on current imaging techniques (Additional file 1), and indicate its significance for early evolution of Holometabola.Fig. 1

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