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Polyphyly of the extinct family Oviparosiphidae and its implications for inferring aphid evolution (Hemiptera, Sternorrhyncha).

ABSTRACT: Aphidoidea, the so-called "true aphids" are one of the most challenging groups in terms of solving the phylogenetic relationships. Morphology-based analyses were strongly affected by widespread homoplasy, while the molecular-based attempts struggled with the lack of sufficient phylogenetic signal. Despite significant improvements, the higher classification still remains unresolved and rather controversial. However, the use of the fossil record, one of the most valuable sources of information, was mainly limited to calibration of a phylogenetic tree, without a direct inclusion into the analysis. The extinct family Oviparosiphidae has long been considered as the common ancestor of all recent Aphidoidea and it was used as a calibration point in several analyses, but it has been never analyzed in a phylogenetic context. The family has been treated as a monophyletic group purely based on the simultaneous presence of two abdominal structures, ovipositor and siphunculi. However, it has been shown recently that at least one more extinct lineage, present at the same time, was characterized by the same features. For these reasons, we performed a maximum parsimony analysis using morphological data for extinct aphid taxa to prove the monophyly of Oviparosiphidae. Our analysis shows that the presumed ancestor lineage of recent aphids is a polyphyletic group. Our results support the hypothesis of an early Mesozoic rapid radiation of aphids, which led to several different lineages characterized by both ovipositor and siphunculi. The results indicate the necessity of examining the other extinct families, and shows that the diversity of aphids before the Cretaceous Terrestrial Revolution (KTR) was higher than expected. Even though there is not enough data to perform a formal analysis, fossils seem to suggest a significant impact of the KTR on aphid diversification. Additionally, we have made a redescription of two genera and description of a new species, Vitimaphis subridens sp. nov.

SUBMITTER: Zyla D

PROVIDER: S-EPMC5405925 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: With some exceptions, mitochondria within the class Insecta have the same gene content, and generally, a similar gene order allowing the proposal of an ancestral gene order. The principal exceptions are several orders within the Hemipteroid assemblage including the order Thysanoptera, a sister group of the order Hemiptera. Within the Hemiptera, there are available a number of completely sequenced mitochondrial genomes that have a gene order similar to that of the proposed ancestor. None, however, are available from the suborder Sternorryncha that includes whiteflies, psyllids and aphids. RESULTS: We have determined the complete nucleotide sequence of the mitochondrial genomes of six species of whiteflies, one psyllid and one aphid. Two species of whiteflies, one psyllid and one aphid have mitochondrial genomes with a gene order very similar to that of the proposed insect ancestor. The remaining four species of whiteflies had variations in the gene order. In all cases, there was the excision of a DNA fragment encoding for cytochrome oxidase subunit III(COIII)-tRNAgly-NADH dehydrogenase subunit 3(ND3)-tRNAala-tRNAarg-tRNAasn from the ancestral position between genes for ATP synthase subunit 6 and NADH dehydrogenase subunit 5. Based on the position in which all or part of this fragment was inserted, the mitochondria could be subdivided into four different gene arrangement types. PCR amplification spanning from COIII to genes outside the inserted region and sequence determination of the resulting fragments, indicated that different whitefly species could be placed into one of these arrangement types. A phylogenetic analysis of 19 whitefly species based on genes for mitochondrial cytochrome b, NADH dehydrogenase subunit 1, and 16S ribosomal DNA as well as cospeciating endosymbiont 16S and 23S ribosomal DNA indicated a clustering of species that corresponded to the gene arrangement types. CONCLUSIONS: In whiteflies, the region of the mitochondrial genome consisting of genes encoding for COIII-tRNAgly-ND3-tRNAala-tRNAarg-tRNAasn can be transposed from its ancestral position to four different locations on the mitochondrial genome. Related species within clusters established by phylogenetic analysis of host and endosymbiont genes have the same mitochondrial gene arrangement indicating a transposition in the ancestor of these clusters.

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Polyphyly of the extinct family Oviparosiphidae and its implications for inferring aphid evolution (Hemiptera, Sternorrhyncha).

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