facultative symbionts, which may affect their function or transmission rates (Corbin
et al. 2017).
Early results show that temperature is a key determinant in the success of
symbiont-mediated defenses. For example, a common aphid symbiont, Hamiltonella
defensa, confers resistance against hymenopteran parasitoids (Vorburger 2014;
Oliver and Higashi 2019). The likely mechanistic basis for these anti-parasitoid
defenses are eukaryotic toxins encoded on a bacteriophage called APSE, with
variable levels of protection depending on the strain (Oliver et al. 2009; Degnan
and Moran 2008; Brandt et al. 2017). However, symbiont protection across a range
of H. defensa/APSE strains has been shown to fail under modest increases (+5–7
C)
in temperature (Doremus et al. 2018).
Most studies investigating the effects of temperature on facultative symbioses
have used either heat shocks or increases that are !5
C above controls and held at
constant temperatures or under diurnal regimens. However, a recent study examined
the effects of just a 2.5
C increase, consistent with near-term IPCC predictions, on
the anti-parasitoid defensive symbiosis in pea aphids (Higashi et al. 2020). This
study also used treatments that mimicked daily fluctuations at the site of aphid
collection by cycling between average daily lows and highs, and varied the timing
of warming because models and empirical findings indicate that nighttime temperatures are increasing faster than daytime temperatures (Davy et al. 2017). Ectothermic animals may respond differently to daytime and nighttime warming as the
former moves organisms nearer to their thermal limits and results in greater daily
temperature variation, while night warming minimizes these, and may even relieve
constraints of cooler nighttime temperatures (Speights et al. 2017). However, the
aphid study found that regardless of the timing of warming
(uniform vs. day vs. night) an increase of just 2.5
C was enough to substantially
decrease symbiont-based protection (Higashi et al. 2020). Surprisingly, the daily
maxima for the no-warming control and nighttime-warming treatments were identical, indicating that higher temperature per se was not the cause of symbiont failure.
Also, while outcomes of host–parasite interactions are often mediated by temperature (Thomas and Blanford 2003), here only symbiotic organisms were harmed by
warming. If this pattern holds for other protective Hamiltonella, then thousands of
aphid species may be more vulnerable to common enemies as the planet warms.
One caveat is that insect symbionts, including aphid defensive symbionts, are
primarily studied in laboratory settings. In the field, many factors, both selective and
nonselective, can influence symbiont dynamics (Oliver et al. 2014). While
Hamiltonella has been shown to confer defensive benefits in the field (Smith et al.
2015; Rothacher et al. 2016; Ives et al. 2020), protective benefits do not appear to be
the only force underlying their prevalence across populations (Smith et al. 2015). A
recent longitudinal field study found that warmer temperatures, not parasitoids, were
the best predictor of Hamiltonella infections throughout a sampled season (Smith
et al. 2020). Some Hamiltonella strains have been shown to confer tolerance to heat
stress, which may be the basis for symbiont persistence in this study (Russell and
Moran 2006; Doremus et al. 2018). While apparently less common than symbiontbased defenses, some pea aphid clones are endogenously resistant to parasitoids, yet
16 Symbiosis in a Rapidly Changing World
275
et al. 2017).
Early results show that temperature is a key determinant in the success of
symbiont-mediated defenses. For example, a common aphid symbiont, Hamiltonella
defensa, confers resistance against hymenopteran parasitoids (Vorburger 2014;
Oliver and Higashi 2019). The likely mechanistic basis for these anti-parasitoid
defenses are eukaryotic toxins encoded on a bacteriophage called APSE, with
variable levels of protection depending on the strain (Oliver et al. 2009; Degnan
and Moran 2008; Brandt et al. 2017). However, symbiont protection across a range
of H. defensa/APSE strains has been shown to fail under modest increases (+5–7
C)
in temperature (Doremus et al. 2018).
Most studies investigating the effects of temperature on facultative symbioses
have used either heat shocks or increases that are !5
C above controls and held at
constant temperatures or under diurnal regimens. However, a recent study examined
the effects of just a 2.5
C increase, consistent with near-term IPCC predictions, on
the anti-parasitoid defensive symbiosis in pea aphids (Higashi et al. 2020). This
study also used treatments that mimicked daily fluctuations at the site of aphid
collection by cycling between average daily lows and highs, and varied the timing
of warming because models and empirical findings indicate that nighttime temperatures are increasing faster than daytime temperatures (Davy et al. 2017). Ectothermic animals may respond differently to daytime and nighttime warming as the
former moves organisms nearer to their thermal limits and results in greater daily
temperature variation, while night warming minimizes these, and may even relieve
constraints of cooler nighttime temperatures (Speights et al. 2017). However, the
aphid study found that regardless of the timing of warming
(uniform vs. day vs. night) an increase of just 2.5
C was enough to substantially
decrease symbiont-based protection (Higashi et al. 2020). Surprisingly, the daily
maxima for the no-warming control and nighttime-warming treatments were identical, indicating that higher temperature per se was not the cause of symbiont failure.
Also, while outcomes of host–parasite interactions are often mediated by temperature (Thomas and Blanford 2003), here only symbiotic organisms were harmed by
warming. If this pattern holds for other protective Hamiltonella, then thousands of
aphid species may be more vulnerable to common enemies as the planet warms.
One caveat is that insect symbionts, including aphid defensive symbionts, are
primarily studied in laboratory settings. In the field, many factors, both selective and
nonselective, can influence symbiont dynamics (Oliver et al. 2014). While
Hamiltonella has been shown to confer defensive benefits in the field (Smith et al.
2015; Rothacher et al. 2016; Ives et al. 2020), protective benefits do not appear to be
the only force underlying their prevalence across populations (Smith et al. 2015). A
recent longitudinal field study found that warmer temperatures, not parasitoids, were
the best predictor of Hamiltonella infections throughout a sampled season (Smith
et al. 2020). Some Hamiltonella strains have been shown to confer tolerance to heat
stress, which may be the basis for symbiont persistence in this study (Russell and
Moran 2006; Doremus et al. 2018). While apparently less common than symbiontbased defenses, some pea aphid clones are endogenously resistant to parasitoids, yet
16 Symbiosis in a Rapidly Changing World
275