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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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Expression domains of abdominal Hox genes in larvae of the earliest holometabolans, the beetle Tribolium castaneum, and other modern taxa. The expression of Ubx, Abd-A and Abd-B Hox genes in larvae of the earliest holometabolans are shown at (a, b). The most closely related model species affiliated with the earliest holometabolans probably is the beetle Tribolium castaneum, whose pattern of Hox gene development is shown in the wild-type at (c), and an Ubx/Abd-A mutant in (d). A sample of the Hox gene effects on abdominal leglet development are given in (e–g), showing the variety of expression patterns on abdominal appendages in taxa of the Hymenoptera, Diptera and Lepidoptera. The expression domains of Distalless (Dll), and the Hox genes Ultrabithorax (Ubx), Abdominal-A (Abd-A) and Abdominal-B (Abd-B) [15] in holometabolous larvae is shown at (h). The colors represent, from anterior to posterior: orange, antennae; green, mouthparts; blue, thoracic legs; red, abdominal leglets; and yellow, cerci. The stemmata likely are present and the cerci are inferred in Srokalarva berthei
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Fig6: Expression domains of abdominal Hox genes in larvae of the earliest holometabolans, the beetle Tribolium castaneum, and other modern taxa. The expression of Ubx, Abd-A and Abd-B Hox genes in larvae of the earliest holometabolans are shown at (a, b). The most closely related model species affiliated with the earliest holometabolans probably is the beetle Tribolium castaneum, whose pattern of Hox gene development is shown in the wild-type at (c), and an Ubx/Abd-A mutant in (d). A sample of the Hox gene effects on abdominal leglet development are given in (e–g), showing the variety of expression patterns on abdominal appendages in taxa of the Hymenoptera, Diptera and Lepidoptera. The expression domains of Distalless (Dll), and the Hox genes Ultrabithorax (Ubx), Abdominal-A (Abd-A) and Abdominal-B (Abd-B) [15] in holometabolous larvae is shown at (h). The colors represent, from anterior to posterior: orange, antennae; green, mouthparts; blue, thoracic legs; red, abdominal leglets; and yellow, cerci. The stemmata likely are present and the cerci are inferred in Srokalarva berthei

Mentions: The placement of serially homologous hexapod segments and their appendages is under the early developmental regulation by discrete clusters of homeotic genes, or Hox genes [16]. Several genes could have regulated the expression or nonexpression of abdominal appendages, such as leglets of Srokalarva berthei (Fig. 4) and Metabolarva bella (Fig. 5) [17]. The gene Distalless (Dll) is responsible for evaginations of the body wall that often result in development of segmental appendages such as certain mouthparts, antennae and walking legs [16]. This general function of Dll, in combination with Hox genes such as abd-A, are commissioned to express or repress development of appendages in certain body regions, such as the ventral abdominal leglet series of segments A1–A8 in many insects [15], unless it is repressed by the Hox genes Ultrabithorax (Ubx), Abdominal-A (abd-A) or their functional equivalents (Fig. 6h) [18]. Repression of Dll by Ubx or abd-A is well documented in a variety of model insects, particularly the holometabolous larvae of the red flour beetle Tribolium castaneum (Coleoptera) (Fig. 6c, d) [15, 19], pomace fly Drosophila melanogaster (Diptera) [20], silkworm Bombyx mori (Lepidoptera) [21], and other holometabolous insects (Fig. 6e–g). These genetic switches are also known for more basal insect lineages such as the cricket Gryllus bimaculatus [22] and grasshopper Schistocerca gregaria (Orthoptera) [23], and more remotely, the springtail Orchesella cincta (Collembola) [24], a non-insect hexapod. Although developmental capacity for expression and repression of abdominal leglets was inherited by the earliest holometabolous lineages [25], it appears that the oldest eruciform larvae had a conservative abdominal Hox-gene developmental pattern, with a complete series of leglets on segments A1–A8 in Srokalarva berthei (Figs. 4, 6a) and A2–A7 in Metabolarva bella (Figs. 5, 6b) the latter indicating that the abd-A gene repressed leglet expression in segment A1.Fig. 5


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)

Expression domains of abdominal Hox genes in larvae of the earliest holometabolans, the beetle Tribolium castaneum, and other modern taxa. The expression of Ubx, Abd-A and Abd-B Hox genes in larvae of the earliest holometabolans are shown at (a, b). The most closely related model species affiliated with the earliest holometabolans probably is the beetle Tribolium castaneum, whose pattern of Hox gene development is shown in the wild-type at (c), and an Ubx/Abd-A mutant in (d). A sample of the Hox gene effects on abdominal leglet development are given in (e–g), showing the variety of expression patterns on abdominal appendages in taxa of the Hymenoptera, Diptera and Lepidoptera. The expression domains of Distalless (Dll), and the Hox genes Ultrabithorax (Ubx), Abdominal-A (Abd-A) and Abdominal-B (Abd-B) [15] in holometabolous larvae is shown at (h). The colors represent, from anterior to posterior: orange, antennae; green, mouthparts; blue, thoracic legs; red, abdominal leglets; and yellow, cerci. The stemmata likely are present and the cerci are inferred in Srokalarva berthei
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig6: Expression domains of abdominal Hox genes in larvae of the earliest holometabolans, the beetle Tribolium castaneum, and other modern taxa. The expression of Ubx, Abd-A and Abd-B Hox genes in larvae of the earliest holometabolans are shown at (a, b). The most closely related model species affiliated with the earliest holometabolans probably is the beetle Tribolium castaneum, whose pattern of Hox gene development is shown in the wild-type at (c), and an Ubx/Abd-A mutant in (d). A sample of the Hox gene effects on abdominal leglet development are given in (e–g), showing the variety of expression patterns on abdominal appendages in taxa of the Hymenoptera, Diptera and Lepidoptera. The expression domains of Distalless (Dll), and the Hox genes Ultrabithorax (Ubx), Abdominal-A (Abd-A) and Abdominal-B (Abd-B) [15] in holometabolous larvae is shown at (h). The colors represent, from anterior to posterior: orange, antennae; green, mouthparts; blue, thoracic legs; red, abdominal leglets; and yellow, cerci. The stemmata likely are present and the cerci are inferred in Srokalarva berthei
Mentions: The placement of serially homologous hexapod segments and their appendages is under the early developmental regulation by discrete clusters of homeotic genes, or Hox genes [16]. Several genes could have regulated the expression or nonexpression of abdominal appendages, such as leglets of Srokalarva berthei (Fig. 4) and Metabolarva bella (Fig. 5) [17]. The gene Distalless (Dll) is responsible for evaginations of the body wall that often result in development of segmental appendages such as certain mouthparts, antennae and walking legs [16]. This general function of Dll, in combination with Hox genes such as abd-A, are commissioned to express or repress development of appendages in certain body regions, such as the ventral abdominal leglet series of segments A1–A8 in many insects [15], unless it is repressed by the Hox genes Ultrabithorax (Ubx), Abdominal-A (abd-A) or their functional equivalents (Fig. 6h) [18]. Repression of Dll by Ubx or abd-A is well documented in a variety of model insects, particularly the holometabolous larvae of the red flour beetle Tribolium castaneum (Coleoptera) (Fig. 6c, d) [15, 19], pomace fly Drosophila melanogaster (Diptera) [20], silkworm Bombyx mori (Lepidoptera) [21], and other holometabolous insects (Fig. 6e–g). These genetic switches are also known for more basal insect lineages such as the cricket Gryllus bimaculatus [22] and grasshopper Schistocerca gregaria (Orthoptera) [23], and more remotely, the springtail Orchesella cincta (Collembola) [24], a non-insect hexapod. Although developmental capacity for expression and repression of abdominal leglets was inherited by the earliest holometabolous lineages [25], it appears that the oldest eruciform larvae had a conservative abdominal Hox-gene developmental pattern, with a complete series of leglets on segments A1–A8 in Srokalarva berthei (Figs. 4, 6a) and A2–A7 in Metabolarva bella (Figs. 5, 6b) the latter indicating that the abd-A gene repressed leglet expression in segment A1.Fig. 5

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