specific pathways that might provide climate resilience, but those retained show
reduced function, especially under stressful conditions.
Take aphids, a group of ca. 5000 phloem-feeding insects, which have a 100+
million-year association with the bacterium Buchnera aphidicola and show genomes
at varying degrees of degradation (Chong et al. 2019). Many Buchnera proteins
show reduced thermal stability compared to free-living relatives and the symbiont
must compensate for this via the constitutive expression of heat-shock chaperones
(DnaK/GroEL) that prevent protein misfolding (van Ham et al. 2003; Fares et al.
2002). These findings suggest that Buchnera limits the thermal tolerance of their
hosts, which has been hypothesized to at least partially explain why aphids are
largely restricted to the temperate northern hemisphere (Perkovsky and Wegierek
2016). Indeed, a recent study finds that aphid species show variation in responses to
heat stress and a key determinant of aphid fitness is the heat sensitivity of Buchnera
(Zhang et al. 2019). Even within aphid species, a single bp change in the promoter of
the Buchnera small heat shock protein IbpA can result in dramatic changes in aphid
and Buchnera fitness at varying temperatures (Zhang et al. 2019; Dunbar et al.
2007). Heat also negatively impacts nutritional symbionts in ants (Fan and
Wernegreen 2013), psyllids (Hussain et al. 2017), roaches (Sacchi et al. 1993),
weevils (Heddi et al. 1999), and whiteflies (Shan et al. 2017).
Most studies documenting the effects of temperature on obligate symbioses have
used brief exposures to high temperatures (i.e., heat shocks). While studies investigating how long-term exposure to warmer mean temperatures will impact obligate
nutritional symbionts are needed, heat shock experiments are also informative as
climate models predict more frequent, intense, and longer maximum temperatures
(Meehl and Tebaldi 2004). Depending on the availability of microclimates and
behavioral responses, tolerance to “new” extremes and temperature variability will
likely be key determinants of the future ranges and viability of arthropods with
obligate symbioses (Woods et al. 2015; Vasseur et al. 2014; Sunday et al. 2014).
Hence, unless compensating mechanisms are employed, obligate partners are
likely to serve as an “Achilles heel,” turning hundred-million-year-old mutualists
into parasites. In contrast to marine organisms, switching to more thermally stable
obligate symbionts is less likely to be a viable general strategy in terrestrial arthropods, in part due to transovarial, rather than environmental, transmission. And, in
general, obligate symbiont switching is rare (Bennett and Moran 2015). Intriguingly
though, the few aphid groups that have lost Buchnera and switched to different
symbionts (bacteria or fungi) reside in tropical and subtropical regions suggesting
switches may have been temperature related (Fukatsu et al. 1994; Chong and Moran
2018; Buchner 1965). For obligate symbionts in terrestrial systems that are environmentally transmitted, symbiont swapping may be a viable tactic. For instance,
herbivorous leafcutter ants inhabit low-to-mid-elevation tropics owing to dependence on a cold-sensitive Attamyces fungus, which they have cultivated for millions
of years as a food source. However, their northernmost limit is expanded by
behaviorally modifying fungal garden depth in conjunction with using cold-tolerant
fungal strains (Mueller et al. 2011).
16 Symbiosis in a Rapidly Changing World
273
reduced function, especially under stressful conditions.
Take aphids, a group of ca. 5000 phloem-feeding insects, which have a 100+
million-year association with the bacterium Buchnera aphidicola and show genomes
at varying degrees of degradation (Chong et al. 2019). Many Buchnera proteins
show reduced thermal stability compared to free-living relatives and the symbiont
must compensate for this via the constitutive expression of heat-shock chaperones
(DnaK/GroEL) that prevent protein misfolding (van Ham et al. 2003; Fares et al.
2002). These findings suggest that Buchnera limits the thermal tolerance of their
hosts, which has been hypothesized to at least partially explain why aphids are
largely restricted to the temperate northern hemisphere (Perkovsky and Wegierek
2016). Indeed, a recent study finds that aphid species show variation in responses to
heat stress and a key determinant of aphid fitness is the heat sensitivity of Buchnera
(Zhang et al. 2019). Even within aphid species, a single bp change in the promoter of
the Buchnera small heat shock protein IbpA can result in dramatic changes in aphid
and Buchnera fitness at varying temperatures (Zhang et al. 2019; Dunbar et al.
2007). Heat also negatively impacts nutritional symbionts in ants (Fan and
Wernegreen 2013), psyllids (Hussain et al. 2017), roaches (Sacchi et al. 1993),
weevils (Heddi et al. 1999), and whiteflies (Shan et al. 2017).
Most studies documenting the effects of temperature on obligate symbioses have
used brief exposures to high temperatures (i.e., heat shocks). While studies investigating how long-term exposure to warmer mean temperatures will impact obligate
nutritional symbionts are needed, heat shock experiments are also informative as
climate models predict more frequent, intense, and longer maximum temperatures
(Meehl and Tebaldi 2004). Depending on the availability of microclimates and
behavioral responses, tolerance to “new” extremes and temperature variability will
likely be key determinants of the future ranges and viability of arthropods with
obligate symbioses (Woods et al. 2015; Vasseur et al. 2014; Sunday et al. 2014).
Hence, unless compensating mechanisms are employed, obligate partners are
likely to serve as an “Achilles heel,” turning hundred-million-year-old mutualists
into parasites. In contrast to marine organisms, switching to more thermally stable
obligate symbionts is less likely to be a viable general strategy in terrestrial arthropods, in part due to transovarial, rather than environmental, transmission. And, in
general, obligate symbiont switching is rare (Bennett and Moran 2015). Intriguingly
though, the few aphid groups that have lost Buchnera and switched to different
symbionts (bacteria or fungi) reside in tropical and subtropical regions suggesting
switches may have been temperature related (Fukatsu et al. 1994; Chong and Moran
2018; Buchner 1965). For obligate symbionts in terrestrial systems that are environmentally transmitted, symbiont swapping may be a viable tactic. For instance,
herbivorous leafcutter ants inhabit low-to-mid-elevation tropics owing to dependence on a cold-sensitive Attamyces fungus, which they have cultivated for millions
of years as a food source. However, their northernmost limit is expanded by
behaviorally modifying fungal garden depth in conjunction with using cold-tolerant
fungal strains (Mueller et al. 2011).
16 Symbiosis in a Rapidly Changing World
273