threatened species, such as the iconic giant clams currently listed as “vulnerable” due
to the overharvesting of their decorative shells.
16.3.2 Obligate Symbionts as “Achilles Heels” for Many
Terrestrial Arthropods?
Invertebrate animals, especially arthropods, dominate terrestrial ecosystems with
respect to diversity, abundance, and ecosystem services. These animals are often
infected with specialized symbionts that play key roles in nutrient acquisition and
host defense (Oliver and Martinez 2014). Early results indicate that GCC may harm
these specialized symbioses in particular, where the loss of function, or of the
symbiont itself, may curtail the distribution of the animal host or its resilience to a
changing climate. For instance, some insects have highly specialized gut symbionts,
such as the southern green stink bug, Nezara viridula, which harbors specific
bacterial symbionts in midgut crypts required for insect development (Tada et al.
2011). Warming treatments of just 2.5
C reduced symbiont abundance and host
fitness to levels similar to those observed for aposymbiotic bugs; while warming of
5
C completely eliminated development to adulthood (Kikuchi et al. 2016). Related
insects have also been shown to lose their specific crypt-associated gut symbionts
with 5
C increases in temperature (Prado et al. 2010) suggesting this phenomenon
may be common for this type of symbiosis.
Most obligate nutritional symbioses, which occur in tens of thousands of terrestrial arthropod species, are even more specialized. For example, most plant
sap-feeding, and many blood-feeding insects, harbor maternally transmitted intracellular symbionts that provision amino acids (sap) or B vitamins (blood) that occur
in insufficient quantities in their respective diets (Vogel and Coon 2020; Moran et al.
2008; Duron et al. 2018). These associations are typically mutually obligate, with
symbionts restricted to host cells (bacteriocytes) and organs (bacteriomes) and
displaying sophisticated metabolic integration and regulation (Wilson 2020;
Buchner 1965; Baumann 2005). Ancient infection with these symbionts provided
numerous arthropod groups with the metabolic machinery to exploit previously
unusable niches, within which they subsequently diversified. However, a lifestyle
restricted to specific host tissues combined with transmission bottlenecks, which
limits effective population sizes, comes with long-term consequences. These include
elevated mutation rates and the accumulation of deleterious mutations; processes
that result in gene inactivation, loss, and eventually extreme genome reduction
(Wernegreen 2017; Moran and Bennett 2014; Bennett and Moran 2015). For
instance, one general pattern is that the large majority of host-restricted organisms,
obligate symbionts included, show degenerated aminoacyl-tRNA synthetase
domains, which can lead to inaccurate translation resulting in a global decline in
protein quality (Melnikov et al. 2018). Not only have obligate symbionts lost
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K. M. Oliver and C. H. V. Higashi
to the overharvesting of their decorative shells.
16.3.2 Obligate Symbionts as “Achilles Heels” for Many
Terrestrial Arthropods?
Invertebrate animals, especially arthropods, dominate terrestrial ecosystems with
respect to diversity, abundance, and ecosystem services. These animals are often
infected with specialized symbionts that play key roles in nutrient acquisition and
host defense (Oliver and Martinez 2014). Early results indicate that GCC may harm
these specialized symbioses in particular, where the loss of function, or of the
symbiont itself, may curtail the distribution of the animal host or its resilience to a
changing climate. For instance, some insects have highly specialized gut symbionts,
such as the southern green stink bug, Nezara viridula, which harbors specific
bacterial symbionts in midgut crypts required for insect development (Tada et al.
2011). Warming treatments of just 2.5
C reduced symbiont abundance and host
fitness to levels similar to those observed for aposymbiotic bugs; while warming of
5
C completely eliminated development to adulthood (Kikuchi et al. 2016). Related
insects have also been shown to lose their specific crypt-associated gut symbionts
with 5
C increases in temperature (Prado et al. 2010) suggesting this phenomenon
may be common for this type of symbiosis.
Most obligate nutritional symbioses, which occur in tens of thousands of terrestrial arthropod species, are even more specialized. For example, most plant
sap-feeding, and many blood-feeding insects, harbor maternally transmitted intracellular symbionts that provision amino acids (sap) or B vitamins (blood) that occur
in insufficient quantities in their respective diets (Vogel and Coon 2020; Moran et al.
2008; Duron et al. 2018). These associations are typically mutually obligate, with
symbionts restricted to host cells (bacteriocytes) and organs (bacteriomes) and
displaying sophisticated metabolic integration and regulation (Wilson 2020;
Buchner 1965; Baumann 2005). Ancient infection with these symbionts provided
numerous arthropod groups with the metabolic machinery to exploit previously
unusable niches, within which they subsequently diversified. However, a lifestyle
restricted to specific host tissues combined with transmission bottlenecks, which
limits effective population sizes, comes with long-term consequences. These include
elevated mutation rates and the accumulation of deleterious mutations; processes
that result in gene inactivation, loss, and eventually extreme genome reduction
(Wernegreen 2017; Moran and Bennett 2014; Bennett and Moran 2015). For
instance, one general pattern is that the large majority of host-restricted organisms,
obligate symbionts included, show degenerated aminoacyl-tRNA synthetase
domains, which can lead to inaccurate translation resulting in a global decline in
protein quality (Melnikov et al. 2018). Not only have obligate symbionts lost
272
K. M. Oliver and C. H. V. Higashi