Microbial symbionts expanding or constraining abiotic niche space in insects

Lemoine, Marion; Engl, Tobias; Kaltenpoth, Martin

doi:10.1016/j.cois.2020.01.003

Cited by 97 publications

(73 citation statements)

References 63 publications

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“…Symbioses play a major role in the ecology and evolution of organisms [ 1 , 2 ]. Microbial symbionts can provide various benefits to their host, from nutrient supplementation and support in food digestion and detoxification to defense against natural enemies and adaptation to abiotic environmental conditions [ 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 ]. However, engaging in a symbiotic association can also be costly.…”

Section: Introductionmentioning

confidence: 99%

Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle

Engl

Schmidt

Kanyile

et al. 2020

Insects

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Animals engage in a plethora of mutualistic interactions with microorganisms that can confer various benefits to their host but can also incur context-dependent costs. The sawtoothed grain beetle Oryzaephilus surinamensis harbors nutritional, intracellular Bacteroidetes bacteria that supplement precursors for the cuticle synthesis and thereby enhance desiccation resistance of its host. Experimental elimination of the symbiont impairs cuticle formation and reduces fitness under desiccation stress but does not disrupt the host’s life cycle. For this study, we first demonstrated that symbiont populations showed the strongest growth at the end of metamorphosis and then declined continuously in males, but not in females. The symbiont loss neither impacted the development time until adulthood nor adult mortality or lifespan. Furthermore, lifetime reproduction was not influenced by the symbiont presence. However, symbiotic females started to reproduce almost two weeks later than aposymbiotic ones. Thus, symbiont presence incurs a metabolic and context-dependent fitness cost to females, probably due to a nutrient allocation trade-off between symbiont growth and sexual maturation. The O. surinamensis symbiosis thereby represents an experimentally amenable system to study eco-evolutionary dynamics under variable selection pressures.

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Section: Introductionmentioning

confidence: 99%

Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle

Engl

Schmidt

Kanyile

et al. 2020

Insects

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“…Pesticides could thus indirectly affect colonization by Snodgrassella and perhaps other key 360 symbionts, a process we have shown to be temperature-sensitive. Whether symbionts indeed 361 constrain (or even improve [85]) bee responses to heat and other stressors remains an important 362 priority for future research, as bees and the pollination services they provide continue to face 363 serious challenges. 364…”

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confidence: 99%

Thermal niches of specialized gut symbionts: the case of social bees

Hammer

Moran

2020

Preprint

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1 2 Responses to climate change are particularly complicated in species that engage in 3 symbioses, as the niche of one partner may be modified by that of the other. We explored 4 thermal traits in gut symbionts of honeybees and bumblebees, which are vulnerable to rising 5 temperatures. In vitro assays of symbiont strains isolated from 16 host species revealed variation 6 in thermal niches. Strains from bumblebees tended to be less heat-tolerant than those from 7 honeybees, possibly due to bumblebees maintaining cooler nests or inhabiting cooler climates. 8Overall however, bee symbionts grew at temperatures up to 44 °C and withstood temperatures up 9 to 52 °C, at or above the upper thermal limits of their hosts. While heat-tolerant, most strains of 10 the symbiont Snodgrassella grew relatively slowly below 35 °C, perhaps because of adaptation 11 to the elevated body temperatures that bees maintain through thermoregulation. In a gnotobiotic 12 bumblebee experiment, Snodgrassella was unable to consistently colonize bees reared below 35 13 °C under conditions that limit thermoregulation. Thus, host thermoregulatory behavior appears 14 important in creating a warm microenvironment for symbiont establishment. Bee-microbiome-15 temperature interactions could affect host health and pollination services, and inform research on 16 the thermal biology of other specialized gut symbionts, such as those of humans. 17 18 19 20 Earth's climate is rapidly warming, and there is an urgent need to understand how 21 organisms will respond [1,2]. One factor complicating such predictions is the role of interspecific 22 interactions [3,4], and, in particular, symbiosis [5,6]. Many organisms closely associate with one 23 or more distantly related partners that have highly distinct physiologies, as in the case of animal 24 or plant hosts and their microbiomes. Hosts and microbes are likely to have different responses 25 to temperature; yet, if they are mutually dependent, the combined niche is restricted to that of the 26 more sensitive partner. Furthermore, thermal niches can themselves evolve in response to 27 symbiotic lifestyles. For example, obligate endosymbionts that undergo strong population 28 bottlenecks during transmission may evolve unstable, easily denatured proteins as a consequence 29 of mutation accumulation, leading to heat sensitivity [7][8][9]. Both of these factors may constrain 30 the combined thermal niche of strongly symbiont-dependent organisms [6,10,11]. There is 31 evidence for symbiont-imposed constraints on host thermotolerance in a variety of invertebrates 32 such as aphids, ants, stinkbugs, corals, and sponges [12][13][14][15][16]. However, the wider prevalence of 33 this phenomenon is unclear, and, in general, we do not know how microbiomes will influence 34 host responses to climate warming. 35The eusocial corbiculate bees (hereafter "social bees") are a particularly important group 36 in which to study symbiont thermal niches and their effects on hosts. This clade, comprising 37 honey bees (Apis), bumb...

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“…Hence, symbiotic microbes can initially expand their host's niche space, but their genome erosion may subsequently constrain their host's evolutionary potential and confine it to a particular ecological niche. While such symbiosisinflicted constraints have been discussed in the context of the host's viable temperature range 51 , they have rarely been considered for biotic niche dimensions, even though previous studies have shown that host plant specialization can be governed by microbial symbionts 52 , determining and limiting the host's dietary niche space.…”

Section: Discussionmentioning

confidence: 99%

Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles

et al. 2020

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Symbiotic microbes can enable their host to access untapped nutritional resources but may also constrain niche space by promoting specialization. Here, we reconstruct functional changes in the evolutionary history of the symbiosis between a group of (semi-)aquatic herbivorous insects and mutualistic bacteria. Sequencing the symbiont genomes across 26 species of reed beetles (Chrysomelidae, Donaciinae) spanning four genera indicates that the genome-eroded mutualists provide life stage-specific benefits to larvae and adults, respectively. In the plant sap-feeding larvae, the symbionts are inferred to synthesize most of the essential amino acids as well as the B vitamin riboflavin. The adult reed beetles' folivory is likely supported by symbiont-encoded pectinases that complement the host-encoded set of cellulases, as revealed by transcriptome sequencing. However, mapping the occurrence of the symbionts' pectinase genes and the hosts' food plant preferences onto the beetles' phylogeny reveals multiple independent losses of pectinase genes in lineages that switched to feeding on pectin-poor plants, presumably constraining their hosts' subsequent adaptive potential.

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Microbial symbionts expanding or constraining abiotic niche space in insects

Cited by 97 publications

References 63 publications

Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle

Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle

Thermal niches of specialized gut symbionts: the case of social bees

Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles

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