Vertical transmission as the key to the colonization of Madagascar by fungus-growing termites?

Abstract

The mutualism between fungus-growing termites (Macrotermitinae) and their mutualistic fungi (Termitomyces) began in Africa. The fungus-growing termites have secondarily colonized Madagascar and only a subset of the genera found in Africa is found on this isolated island. Successful long-distance colonization may have been severely constrained by the obligate interaction of the termites with fungal symbionts and the need to acquire these symbionts secondarily from the environment for most species (horizontal symbiont transmission). Consistent with this hypothesis, we show that all extant species of fungus-growing termites of Madagascar are the result of a single colonization event of termites belonging to one of the only two groups with vertical symbiont transmission, and we date this event at approximately 13 Mya (Middle/Upper Miocene). Vertical symbiont transmission may therefore have facilitated longdistance dispersal since both partners disperse together. In contrast to their termite hosts, the fungal symbionts have colonized Madagascar multiple times, suggesting that the presence of fungus-growing termites may have facilitated secondary colonizations of the symbiont. Our findings indicate that the absence of the right symbionts in a new environment can prevent long-distance dispersal of symbioses relying on horizontal symbiont acquisition.

Frontier mutualism: coevolutionary patterns at the northern range limit of the leaf-cutter ant–fungus symbiosis

“…Such long-distance dispersal ability of Attamyces would contrast with the dispersal ability of Termitomyces fungi of the termiteTermitomyces symbiosis, in which effective long-distance dispersal of Termitomyces across oceanic barriers appears to be rare (e.g. between mainland Africa and Madagascar [60]). However, long-distance dispersal and genetic mixing of Attamyces could help explain the much younger coalescence and origin of Attamyces fungi (about 2-4 Myr old) compared with the corresponding origin of leaf-cutter ants (about 8 -12 Myr old) [40].…”

Repeated colonization of remote islands by specialized mutualists

“…Island angiosperms are predominantly pollinated by wind or generalist insects and depend on generalist vertebrates for fruit dispersal [4]. Difficulties of synchronous co-establishment are thought to also restrict island colonization by plants or animals that require specialized fungal symbionts [5,6]. Alternatively, specialized mutualisms may be lost when plants colonize islands in the absence of mutualists [7,8].…”

Diversity, population genetics, and evolution of macrofungi associated with animals

“…Indeed, such a pattern has been observed in several studies. For example, the single colonization of Termitomyces fungi in Madagascar was likely established through this mechanism (Nobre 2010a; Nobre et al 2010b). In addition, Nobre et al (2011b) found that the genetic structure of symbiotic fungi of Macrotermes bellicosus is consistent with clonal reproduction with limited evidence for recombination (Table1).…”