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, 11 (6), e0156847
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Oligocene Termite Nests With In Situ Fungus Gardens From the Rukwa Rift Basin, Tanzania, Support a Paleogene African Origin for Insect Agriculture

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Oligocene Termite Nests With In Situ Fungus Gardens From the Rukwa Rift Basin, Tanzania, Support a Paleogene African Origin for Insect Agriculture

Eric M Roberts et al. PLoS One.

Abstract

Based on molecular dating, the origin of insect agriculture is hypothesized to have taken place independently in three clades of fungus-farming insects: the termites, ants or ambrosia beetles during the Paleogene (66-24 Ma). Yet, definitive fossil evidence of fungus-growing behavior has been elusive, with no unequivocal records prior to the late Miocene (7-10 Ma). Here we report fossil evidence of insect agriculture in the form of fossil fungus gardens, preserved within 25 Ma termite nests from southwestern Tanzania. Using these well-dated fossil fungus gardens, we have recalibrated molecular divergence estimates for the origins of termite agriculture to around 31 Ma, lending support to hypotheses suggesting an African Paleogene origin for termite-fungus symbiosis; perhaps coinciding with rift initiation and changes in the African landscape.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Location and stratigraphy of the trace fossil locality, Tanzania.
(A) Location of Tanzania within Africa. (B) Digital elevation model for the study area in the southern end of the Rukwa Rift Basin (white box is shown in C). (C) Geologic map of the Songwe Valley in the southern end of the Rukwa Rift Basin, showing stratigraphy and age of fossil locality. Modified from [18]. (D) Measured section and magnetic stratigraphy through the Nsungwe Formation Type Section, with location of fossil locality shown. Modified from [18]. (E) Photograph of the nest locality in a steeply dipping cliff face along the Nsungwe River. (F, G) Sketch maps of fossil locality showing the orientation and distribution of the termite colonies 1 (RRBP-08248) and 2 (RRBP-15106), with letters corresponding to the different nest chambers in each colony.
Fig 2
Fig 2. Fossil termite nest and fungus comb with comparative Holocene-Recent examples.
(A) In situ fossil termite nest (Vondrichnus planoglobus; RRBP-08248a) with Microfavichnus alveolatus fungus comb trace fossil inside. (B) Backscatter electron (BSE) image of fossilized mylosphere with homogeneous composition of 5–10 μm macerated cellulose and calcified tracheids (elongated cells from the xylem of vascular plants). Inset: Scanning electron microscope (SEM) image of Microfavichnus in (A) showing compressed mylospheres and clay infill. (C, D) Photograph (C) and cartoon (D) of cross-section of RRBP-08248a (A). (E) Holocene fungus chamber with fungus comb, near the Galula Village along the Songwe River, Tanzania. (F) Modern Microtermes fungus comb, Malaysia (photo: Termite Web). Inset: Modern Macrotermes fungus comb.
Fig 3
Fig 3. Photographs of specimens in situ displaying different morphologies and weathering stages.
(A) Sample RRBP 08248a (Colony 1) with preserved fungus comb. (B) Sample RRBP 08248c (Colony 1). (C) Sample RRBP 08248g showing galleries and concentric chambers (Colony 1). (D) Uncollected nest RRBP 08248d (Colony 1) showing an external morphology and gallery network above the main nest.
Fig 4
Fig 4. Structure and composition of preserved mylospheres from Macrotermitinae chamber.
(A) Image of polished surface from sample RRBP 08248g (Colony 1) exposing compressed mylospheres (white) near the nest wall and detrital sediment (dark red) filling the chamber. Morphologies and chemical compositions were analyzed via energy dispersive spectroscopy (EDS) and backscattered electron imaging (BSE) by electron probe microanalysis. The sediment surrounding the mylospheres is clay-rich and contains occasional detrital quartz and feldspar grains (and accessory minerals such as monazite), deposited as the nest walls were expanded and/or through infilling of the chamber during construction of or later burial of the nest. There is a small presence of diagenetic Fe-, Mn-, and Ti-rich cement. (B) BSE image of a mylosphere from (A) revealing a homogeneous composition. Filled and hollow subcylindrical, 5–10 μm particles with a major Ca component comprise the mylospheres. We interpret the mylospheres to be composed of wood fragments now replaced by calcium carbonate, preserving the remnants of macerated cellulose and tracheids (Fig 2B).
Fig 5
Fig 5. Temporal and spatial distribution of fossil termite nests and fungal gardens in Africa.
Colored numbers represent termite trace fossil locations, along with the locality name and taxa present (*represents trace fossil localities with unequivocal fungal gardens associated with termite nests, demonstrating termite agriculture). Numbering refers to stratigraphic position as noted in reference to the Cenozoic time scale (at left). References: 1. Sossus Sand, Namibia [39]; 2. Namaqualand, South Africa [39]; 3. Kolle and Koro-Toro, Chad [11]*; 4. Laetoli, Tanzania [41, 43]; 5. Toros Menala and Kossom Bougoudi, Chad [11]*; 6. Bakate Formation, Ethiopia [44]; 7. Nsungwe Formation, Tanzania (this report)*; 8. Jebel Qatranii Formation, Egypt [14]; 9. Upper Sarir Formation, Libya [15]. 10. Qasr el Sagha Formation, Egypt [14].
Fig 6
Fig 6. Schematic genus-level phylogeny [7, 9] of fungus-growing termites (Macrotermitinae) with recalibrated molecular divergence dates and confidence intervals from Table 1.
This figure is based on simulation 1 and more highly resolved species trees can be found in the S1–S5 Figs. Representatives of the genera Allodontermes, Synacanthotermes and Protermes (faded branches) were not included in the time estimates. Images depict representative fungus combs of the different genera. Sketches of Microtermes and Allodontermes fungal combs from [45] and Ancistrotermes from [46]. Note: the calibration point on the Macrotermes branch corresponds to the age of the ancestor of Macrotermes jeanneli [41].

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Grant support

This research was supported by the US National Science Foundation (NSF EAR_0617561, EAR_0854218, EAR 0933619), National Geographic Society (CRE), and funding from Ohio University and James Cook University. TN was supported by a Marie Curie fellowship (FP7-PEOPLE-2012-CIG Project Reference 321725) and by the Portuguese Foundation for Science and Technology (SFRH/BCC/52187/2013).
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