[Seminar Blog] Genetic accommodation in a heating world

written by: Lasair ni Chochlain

Climate change is something that we are all worried about. But as scientific researchers, linking fields as disparate in focus as evolutionary development and global change is quite a challenge. Dr. Yui Suzuki from Wellesley College is helping to pioneer this interdisciplinary research area by exploring how climate change may shape insect evolution and development. The UMD Department of Entomology hosted Dr. Suzuki for a talk on his research as well as a talk on his experience as a liberal arts professor on August 30, 2024.

Most insects are ectotherms or “cold-blooded” animals, meaning that they rely primarily on the environment for heat. Many scientists have observed a decrease in ectotherm body size in response to temperature (Atkinson, 1994; Daufresne et al., 2009; Sheridan & Bickford, 2011). Dr. Suzuki’s lab is interested in exploring how juvenile hormone (JH) may modulate temperature response in insects. Juvenile hormone is an important regulatory hormone in most (but not all) insects. Manduca sexta, or the tobacco hornworm, is an insect species (and model “system”) commonly used for studies in evolutionary development. It has been used previously to show how growth is regulated (Nijhout & Williams, 1974, Nijhout et al., 2006). In insects such as the tobacco hornworm, JH, along with other endocrine signals, plays a large role in body-size regulation. Dr. Suzuki was interested in how temperature might impact this relationship. This is a pressing concern because as climate change increases, we expect to see extremely high temperatures becoming more common in more parts of the world. 

Fig. 1: The growth trajectories of Manduca sexta at different temperatures, showing the faster growth and smaller peak larval size of M. sexta at 30ºC versus at 20ºC (Suzuki unpublished presentation used with permission, 2024).

Suzuki lab, story # 1 (the temperature size rule) 

​Dr. Suzuki’s lab was able to reaffirm that temperature plays a significant role in Manduca sexta development. At lower temperatures, M. sexta larvae grow more slowly but end up significantly larger. At warmer temperatures, they grow faster but they end up smaller. 

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JH also plays a significant role in larval development. When the M. sexta larvae is at or above a ‘critical weight,’ JH secretion stops and, once completely cleared from the hemolymph, larval growth stops. The Suzuki lab’s question was: is there a relationship between temperature and JH?  They uncovered two pieces of evidence to suggest that JH production and clearance vary significantly at different temperatures. The first is that the gene Kruppel homolog 1 (Kr-h1) is expressed less at higher temperatures. (Hirsch et al., submitted) This gene encodes a critical transcription factor that mediates the JH response and can be used as a proxy for JH concentration. (Minakuchi et al., 2009). The second finding is that in M. sexta larvae, the activity of Juvenile hormone esterase (JHE), a JH degradation enzyme, increased at higher temperatures (Hirsch et al., submitted). Thus, at higher temperatures, JH activity declines and this in turn results in earlier cessation of larval feeding. The temperature size rule therefore seems to be at least partially mediated by JH.

Suzuki lab, story #2 (genetic accommodation and micro-evolution)
Now how do we connect the temperature size rule to climate change? In his presentation. Dr. Suzuki did this by talking about micro-evolution and specifically, genetic accommodation.
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Genetic accommodation is a relatively new theory of adaptive evolution proposed by MJ West Eberhard in 2003. It builds upon Waddington’s theory of genetic assimilation, proposed in 1953. Genetic assimilation is when a phenotype resulting from a response to an environmental condition is expressed without the original environmental input. Genetic accommodation differs from assimilation in several important aspects, a main one being that it can apply to traits that arise out of mutations as well as environmental pressures. Generally, genetic accommodation can be defined as “the process by which a novel phenotype becomes established in a population through polygenic changes in the genetic background, driven by selection on phenotypic variants that are produced by either mutation or environmental change.” (Nijhout & Suzuki, 2008)

Fig 2. The above figure illustrates the concepts of genetic accommodation and assimilation and where they overlap and differ (Ehrenreich & Pfennig, 2016).

Polyphenism is the phenomenon of a single genotype producing two or more distinct genotypes in response to different environmental conditions, and it is one important source of phenotypic plasticity. One example from the insect world is the oat catkin caterpillar, whose morphology depends on whether their larval diet is composed of leaves, which are high in tannin, or catkins, which are low in tannin. The high-tannin-fed caterpillars develop into twig morphs, whereas low-tannin-fed caterpillars develop into catkin morphs (Greene 1989). 

Fig 3. Photographs showing the different morphology of the two morphs of the oatkin caterpillar (Greene, 1989).

Fig. 4. Summary of phenotypic response to environment and genetic accommodation and assimilation of the new black phenotype in M. sexta. (Suzuki and Nijhout, 2006)

This brings us back to the Suzuki lab who utilized a polyphenism in M. sexta larvae to study how the evolutionary processes of genetic accommodation and assimilation operate under high temperatures. The specific polyphenism studied was a variation in larval body color. Figure 4 (A) shows the population prior to the enabling mutation; phenotypic variation is low, and larvae are wildtype in color irrespective of temperature. The enabling mutation leads to a black mutant type shown in (B). Larvae can still develop with the wildtype body color when subjected to heat shocks. After several successive generations, the population became polyphenic (C), with both body colors possible for the population, depending on temperature, displaying the phenomenon of genetic accommodation. Finally, (D) shows a monophenic population where the black mutant phenotype has become stable in the population and is evident even at low temperatures, such that genetic assimilation has occurred (Suzuki and Nijhout, 2006). These phenotypic variations were correlated with JH activity. Thus, temperature and JH can modulate phenotype, and this can lead to changes in insect population structures as the climate warms.
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Broad takeaways
Climate change and the corresponding environmental changes may interact with existing genetic variation to shape future evolutionary success. The figure below (Fig. 5) visualizes the impact of climate change on development and the resultant effects on populations and the ecosystem. The degree to which populations can acclimate and adapt will determine whether they will thrive in a heating world. The Suzuki lab showed that developmental hormones can influence how ecological changes affect biology and development. The Suzuki lab has done a lot of work to unravel these processes but, of course, there are many questions still to be answered. 

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Fig 5. This figure illustrates the feedback loop between environmental changes, population changes, and organismal changes. (Suzuki and Toh 2021)

References
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Atkinson, D. (1994). Temperature and Organism Size–A Biological Law for Ectotherms? Advances in Ecological Research 25, https://doi.org/10.1016/S0065-2504(08)60212-3.
 
Daufresne, M., Lengfellner, K., Sommer, U. (2009). Global warming benefits the small in aquatic ecosystems. PNAS 106, no. 31, 12788-12793. https://doi.org/10.1073/pnas.0902080106.
 
Hannah E. Hirsch, Hana Nagata, Laura Park, Mia Hamaguchi, Kamya Chakravarthi, Frederik H. Nijhout, Yuichiro Suzuki. (2024). The role of juvenile hormone in mediating the temperature-size rule in the tobacco hornworm, Manduca sexta. [Manuscript submitted]
 
Nijhout, H. F., Davidowitz, G., & Roff, D. A. (2006). A quantitative analysis of the mechanism that controls body size in Manduca sexta. Journal of biology, 5(5), 16. https://doi.org/10.1186/jbiol43.
 
Nijhout, H. F., & Suzuki, Y. (2008). Environment and genetic accommodation. Biological Theory, 3(3), 204–212. https://doi.org/10.1162/biot.2008.3.3.204. 
 
Nijhout, H. F., & Williams, C. M. (1974). Control of Moulting and Metamorphosis in the Tobacco Hornworm, Manduca Sexta (L.): Cessation of Juvenile Hormone Secretion as A Trigger for Pupation. Journal of Experimental Biology, 61(2), 493–501. https://doi.org/10.1242/jeb.61.2.493.
 
Ehrenreich, Ian M., Pfennig, David W. (2016). Genetic assimilation: a review of its potential proximate causes and evolutionary consequences. Annals of Botany, 117(5), 769–779. https://doi.org/10.1093/aob/mcv130.
 
Greene, E. (1989). A diet-induced development polymorphism in a caterpillar. Science (American Association for the Advancement of Science), 243(4891), 643-646. https://doi.org/10.1126/science.243.4891.643.
 
Minakuchi, C., Namiki, T., Shinoda, T. (2009). Krüppel homolog 1, an early juvenile hormone-response gene downstream of Methoprene-tolerant, mediates its anti-metamorphic action in the red flour beetle Tribolium castaneum. Developmental Biology, 325, 341-350. https://doi.org/10.1016/j.ydbio.2008.10.016.
 
Sheridan, J. and Bickford, D. (2011). Shrinking body size as an ecological response to climate change. Nature Clim Change, 1, 401–406. https://doi.org/10.1038/nclimate1259.
 
Suzuki Y, Nijhout HF. (2006). Evolution of a polyphenism by genetic accommodation. Science. 311(5761):650-2. https://doi.org/10.1126/science.1118888
 
 
Suzuki Y. and Toh L. (2021) Constraints and Opportunities for the Evolution of Metamorphic Organisms in a Changing Climate. Front. Ecol. Evol. 9:734031. https://doi.org/10.3389/fevo.2021.734031.