Evolution, ecology and genomics of invertebrate symbiosis
Parasitoid wasp stinging an aphid to lay an egg within it's body - facultative symbionts have been shown to protect against this parasitic behaviour. Photo by Alex Wild Photography.
Bacterial symbionts are widespread in animals and often provide beneficial functions that profoundly influence their hosts’ biology. Many hosts rely on obligate symbionts to synthesise nutrients absent in their diets. Additionally, numerous symbiotic relationships have now been discovered where the symbiont is not essential for host survival but can provide their host with significant benefits. These are known as facultative symbioses and can confer benefits to the host such as protection against environmental stresses or help them exploit novel resources.
We aim to understand how facultative symbionts help hosts adapt to fluctuating environmental pressures, such as attack from natural enemies, host plant utilisation or heat stress. Using aphids and their facultative symbionts as a model we are asking three key questions:
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Do facultative symbionts act as a ‘horizontal gene pool’ – a reservoir of adaptations carried by symbionts that insects draw from to rapidly adapt to changing environments?
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Why are some host species highly enriched with facultative symbionts, yet other closely related species rarely host them?
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What is the genomic basis of symbiont-derived adaptive traits, such as protection from pathogens and plant exploitation by their insect hosts?
Facultative microbes in host adaptation
Associated Publications
Wu T, Monnin D, Lee RAR, Henry LM (2022). Local adaptation to hosts and parasitoids shape Hamiltonella defesa genotypes across aphid species. Proceeding of the Royal Society, Series B. 298:20221269.
McLean AHC, Godfray HCJ, Ellers J, Henry LM (2019). Host relatedness influences the composition
of aphid microbiomes . Environmental Microbiology Reports 11:808-816.
Niepoth N, Ellers J, Henry LM (2018). Symbiont interactions with non-native hosts limit the
formation of new symbioses. BMC Evolutionary Biology 18:1-12.
Henry LM, Maiden MCJ, Ferrari J, Godfray HCJ ( 2015 ). Insect life history and the evolution
of bacterial mutualism. Ecology Letters 18:516 - 525.
Henry LM, Peccoud J, Simon J-C, Hadfield JD, Maiden MJC, Ferrari J, Godfray HCJ (2013). Horizontally transmitted symbionts and host colonization of ecological niches . Current Biology 23:1713 - 1717.
Evolutionary transitions to obligate symbioses
FISH image showing the localisation of obligate symbiont Buchnera aphidicola (green) and co-obligate symbiont Serratia symbiotica (red) in a Periphyllus aphid. Aphid photo by Influential Points.
Over time, host and symbiont can become so tightly associated that they combine to form a new, more complex life form. This type of extreme symbiotic dependence has resulted in some of the most important evolutionary transitions including the origins of the eukaryotic cell, mitochondria and chloroplast. However, we currently know little about what promotes the stability of these relationships, and how hosts and symbionts integrate over time at a molecular and cellular level.
We seek to understand the metabolic, genomic and cellular changes that occur as a host and symbiont integrate into a new higher-level organism. Invertebrates offer unique insight into the development of these relationships as they have repeatedly evolved obligate dependence on endosymbionts. Our results suggest that the integration of a new symbiont proceeds in a predictable manner – through parallel evolutionary processes (Monnin et al 2020). We now aim to gain a mechanistic and functional understanding of the initial changes that occur when hosts evolve dependence on a microbe, to the advanced integration of an ancient obligate symbiont.
To achieve this aim, we are comparing diverse lineages of annelids, ants and aphids that have evolved obligate and co-obligate symbioses. Key questions we are investigating include:
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What are the step-wise transcriptional and cellular changes that occur as host and symbiont integrate over evolutionary time?
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What initial gene losses bind host and symbionts into dependence?
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What are the genetic mechanisms involved in host control over symbionts?
Associated Publications
Monnin D, Jackson R, Kiers ET, Bunker M, Ellers J, Henry LM (2020). Parallel Evolution in the Integration of a Co-obligate Aphid Symbiosis. Current Biology 30:1949-1957.
Jackson R, Henry LM, Wurm Y (2020) Evolution: the legacy of endosymbiosis in ants. Current Biology 30:PR1385. 10.1016/j.cub.2020.09.023
Fisher RM, Henry LM, Cornwallis CK, Kiers ET, West SA (2017) The evolution of host-symbiont dependence. Nature Communications 8:15973.
Trophic symbioses in host niche use and diversity
Insect phylogeny showing families that have evolved obligate symbioses (blue branches) and those that have not (black) in different feeding niches (coloured nodes). Figure from Cornwallis et al. (in review).
Trophic symbioses – where microbes provide hosts with key resources – have shaped life on earth, from the eukaryotic cell and photosynthesis to deep-sea vent ecosystems, coral reefs, and herbivory. In each case, it is thought that symbionts helped drive the success of their hosts, by allowing the exploitation of novel sources of energy, nutrients and ecologies. Yet, we still have a limited understanding of how and why these relationships evolve, and in many cases, how they impact the diversification of their host.
Here, we are using the recurrent evolution of trophic symbiosis across the insects, and within ants in particular, to better understand the causes and consequences of these relationships. Here we are comparing symbiotic and non-symbiont carrying insect lineages to ask the following questions:
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Are there key limiting nutrients that underlie the evolution of trophic symbioses across diverse taxa?
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What are the costs to the host of evolving dependence on microbes for nutrients?
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How does evolving dependence on microbes impact host diversification?
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Do symbiont acquisitions explain the evolution of extreme feeding specialisation in ants?
Associated Publications
Jackson R, Monnin D, Patapiou P, Golding G, Helanterä H, Oettler J, Heinze J, Wurm Y, Economou C, Chapuisat M, Henry LM (2022) Convergent evolution of a nutritional symbiosis in ants. ISME 16:2114-2122
DOI: 10.1038/s41396-022-01256-1
Cornwallis C, van't Padje A, Ellers J, Klein M, Jackson R, Kiers T, West S, Henry LM (in review) Symbiont-driven niche expansion shaped the adaptive radiation of insects.
DOI: 10.21203/rs.3.rs-1063949/v1
Martín-Durán J, Moggioli G, Panossian B, Sun Y, Thiel D, Martin-Zamora F, Tran M, Clifford A, Goffredi S, Rimskaya-Korsakova N, Jekely G, Tresguerres M, Qian PY, Qiu JW, Rouse G, Henry LM (in review) Distinct genomic routes underlie transitions to specialised symbiotic lifestyles in deep sea annelid worms. Pre-print available at: DOI: 10.21203/rs.3.rs-2049397/v1