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Aphid–Buchnera–Ant symbiosis; or why are aphids rare in the tropics and very rare further south?

Published online by Cambridge University Press:  09 January 2018

Evgeny Perkovsky*
Affiliation:
Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, ul. Bogdana Khmel'nitskogo 15, Kiev 01601, Ukraine. Email: [email protected]
Piotr Wegierek
Affiliation:
Department of Zoology, University of Silesia, Bankowa 9, 40-007 Katowice, Poland. Email: [email protected]
*
*Corresponding author

Abstract

At least since the Cretaceous Terrestrial Revolution, the geographical distribution of aphids, particularly in the Northern Hemisphere, has been strongly affected by the low thermal tolerance of their obligatory bacterial symbiont, Buchnera aphidicola, which was why the aphids switched to obligate parthenogenesis in low latitudes. Hormaphidids and greenideids penetrated into the tropics only after the Oligocene strengthening of climate seasonality, and specialisations of the tropical representatives of these families did not allow them to spread further south (in the case of cerataphidines), or only allowed in few cases (in the case of greenideids).

Aphids suffered from the Mesozoic–Cenozoic boundary extinction event much more strongly than other insects. The extinction was roughly coincidental with the establishment of the tight symbiosis of aphids with formicine and dolichoderine ants, which was accompanied by the flourishing of all three groups.

In the Cretaceous, all of the representatives of extant and subfamilies occupied positions that were subordinate to Armaniinae and Sphecomyrminae. Prior to large ant colonies evolving their efficient ant–aphid mutualism, the aphids remained unprotected before the growing ant predation. The origin of the aphid trophobiosis with large colonies of Formicinae and Dolichoderinae has resulted in the steep decline of aphids left beyond that ant–aphid symbiotic network. By at least the basal Eocene (unlike the Late Cretaceous), ant proportions in the entomofauna increased sharply, and evident dominants emerged. Even now, aphid milkers from small colonies (hundreds of specimens) never protect their symbionts, and homopteran-tending ants are more likely to be dominant, with large colonies of 104–105 workers.

The mutualistic ant–aphid system failed to cross the tropical belt during the Cenozoic because of Buchnera's low heat tolerance. As a result, the native southern temperate aphid fauna consists now of seven genera only, five of which are Late Cretaceous relicts. Some of them had relatives in Late Cretaceous amber of the Northern Hemisphere.

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Copyright © The Royal Society of Edinburgh 2018 

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