Secret infidelities: Ecological processes and the illusion of “apparent species-specificity”

Objectives

  • Understand how host-symbiont associations are maintained
  • Determine ecological processes that maintain partner fidelitymodel

Partner fidelity stabilizes mutualisms over evolutionary time. Partner fidelity is known in many well-studied obligate mutualisms, such as fungus farming in ants , wasps , and beetles . Such observations often tempt researchers to assume that these mutualisms are species-specific; i.e. alternative species combinations cannot “work”. Despite being a crucial element of commonly cited models of symbiosis evolution, species-specificity is rarely tested. Moreover, efforts to relate the evolutionary histories of hosts and symbionts often fail to uncover a shared co-phylogeny , and extensive observational studies often uncover infidelity in associations previously assumed to be species-specific.

In the ambrosia mutualism, beetles feed on their fungi, while fungi are dispersed by their beetles. Fungi are dispersed as pure, growing cultures held  within a highly specialized glandular organ called the mycangium (See video below!). For the symbiosis to “work”, 1) beetles must be able to consume and develop with a particular fungus, and 2) a fungus must be able to invade and proliferate within the mycangium. Working this year with the black twig borer (Xylosandrus compactus), a globally distributed agricultural pest, we have developed novel methods to maintain breeding laboratory colonies of ambrosia beetles and rear beetles in experimental wooden galleries with alternative fungal partners. The black twig borer model system has already provided the first unambiguous demonstration that ambrosia symbioses are not species-specific (Figure below). Black twig borers can feed and develop on multiple ambrosia species, and various ambrosia fungi can invade and proliferate within the black twig borer’s mycangium organ.

 

mycangium
All available published accounts relate the black twig borer to a single ambrosial partner, Ambrosiella xylebori. However, black twig borers often co-infest trees with closely related beetles that farm alternative Ambrosiella species, providing frequent opportunity for symbiont switching. So how do ambrosia beetles maintain apparently species-specific relationships with fungi?

Ecological theory predicts that competitive interactions among potential symbionts are prevalent in mutualisms. Perhaps fungi specialize on specific
hosts, adapting to the particulars of their galleries or mycangia, becoming competitive dominants over alternative symbionts. Perhaps changes in context, such as species invasion to new habitats, result in shifting competitive abilities, leading to occasional host swapping and the observed discord among host and symbiont phylogenies. My work uses the black twig borer model system to explore the ecological mechanisms that underlie apparent species-specificity in mutualisms. Future efforts will use experimental galleries to examine competition among potential symbionts within the gallery and mycangium, and expand to incorporate beetle and fungal species from multiple independent evolutionary origins of ambrosia farming.

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