Chen Hou

Different life histories result in different strategies to allocate energy in biosynthesis, including growth and reproduction, and somatic maintenance. One of the most notable life history differences between Lepidoptera and Blattodea species is that the former grow much faster than the latter, and during metamorphosis, a large amount of tissue in Lepidoptera species disintegrates. In this review, using Lepidoptera caterpillars and cockroach nymphs as examples, we show that, due to these differences in growth processes, cockroach nymphs spend 20 times more energy on synthesizing one unit of biomass (indirect cost of growth) than butterfly caterpillars. Because of the low indirect cost of growth in caterpillars, the fraction of metabolic energy allocated to growth is six times lower, and that for maintenance is seven times higher in caterpillars, compared to cockroach nymphs, despite caterpillar’s higher growth rates. Moreover, due to the higher biosynthetic energy cost in cockroach nymphs, they have better cellular qualities, including higher proteasomal activity for protein quality control and higher resistance to oxidative stress. We also show that under food restriction conditions, the fraction of assimilated energy allocated to growth was reduced by 120% in cockroach nymphs, as they lost body weight under food restriction, while this reduction was only 14% in hornworms, and the body mass increased at a lower rate. Finaly, we discuss future research, especially the difference in adult lifespans associated with the energetic differences.

Evolutionary biology is poised for a third major synthesis. The first presented Darwin's evidence from natural history. The second incorporated genetic mechanisms. The third will be based on energy and biophysical processes. It should include the equal fitness paradigm (EFP), which quantifies how organisms convert biomass into surviving offspring. Natural selection tends to maximise energetic fitness, , where is mass‐specific rate of cohort biomass production, is generation time, is fraction of cohort production that is passed to surviving offspring, and is energy density of biomas. At steady state, parents replace themselves with offspring of equal mass‐specific energy content, ≈ 22.4 kJ/g, and biomass, ≈ 1 g/g. The EFP highlights: (i) the energetic basis of survival and reproduction; (ii) how natural selection acts directly on the parameters of ; (iii) why there is no inherent intrinsic fitness advantage for higher metabolic power, ontogenetic or population growth rate, fecundity, longevity, or resource use efficiency; and (iv) the role of energy in animals with a variety of life histories. Underlying the spectacular diversity of living things is pervasive similarity in how energy is acquired from the environment and used to leave descendants offspring in future generations.

Evolutionary biology is poised for a third major synthesis. The first presented Darwin’s evidence from natural history. The second incorporated genetic mechanisms. The third will be based on energy and biophysical processes. It should include the equal fitness paradigm (EFP), which quantifies how organisms convert biomass into surviving offspring. Natural selection tends to maximize energetic fitness, E=P_coh GFQ, where P_coh is mass-specific rate of cohort biomass production, G is generation time, F is fraction of cohort production that is passed to surviving offspring, and Q is energy density of biomas. At steady state, parents replace themselves with an exactly equal mass-specific energy content, E ≈ 22.4 kJ/g, and biomass, M ≈ 1 g/g, of offspring. The EFP highlights: i) the energetic basis of survival and reproduction; ii) how natural selection acts directly on the parameters of M; iii) why there is no inherent intrinsic fitness advantage for higher metabolic power, ontogenetic or population growth rate, fecundity, longevity, or resource use efficiency; and iv) the role of energy in animals with a variety of life histories. Underlying the spectacular diversity of living things is pervasive similarity in how energy is acquired from the environment and used to leave descendants offspring in future generations.

The comparative studies of aging have established a negative correlation between Gompertz postnatal growth constant and maximum lifespan across mammalian species, but the underlying physiological mechanism remains unclear. This study shows that the Gompertz growth constant can be decomposed into two energetic components, mass-specific metabolic rate and the energetic cost of biosynthesis, and that after controlling the former as a confounder, the negative correlation between growth constant and lifespan still exists due to a 100-fold variation in the latter, revealing that the energetic cost of biosynthesis is a link between growth and longevity in mammals. Previously, the energetic cost of biosynthesis has been thought to be a constant across species and therefore was not considered a contributor to the variation in any life history traits, such as growth and lifespan. This study employs a recently proposed model based on energy conservation to explain the physiological effect of the variation in this energetic cost on the aging process and illustrates its role in linking growth and lifespan. The conventional life history theory suggested a tradeoff between growth and somatic maintenance, but the findings in this study suggest that allocating more energy to biosynthesis may enhance the somatic maintenance and extend lifespan and, hence, reveal a more complex nature of the tradeoff.

Animals with different life histories budget their intake energy differently when food availability is low. It has been shown previously that hornworm (larva of Manduca sexta), a holometabolous insect species with a short development stage, prioritizes growth at the price of metabolism under food restriction, but it is unclear how hemimetabolous insect species with a relatively long development period budget their intake energy under food scarcity. Here, we use orange head cockroaches (Eublaberus posticus) to investigate this question. We found that for both species under food restriction, rates of metabolism and growth were suppressed, but the degree of reduction was more severe in growth than that of metabolism for cockroaches. Under both free-feeding and food restriction conditions, hornworms allocated a larger fraction of assimilated energy to growth than to metabolism, and cockroaches were the opposite. More importantly, when food availability was low, the fraction of assimilated energy allocated to growth was reduced by 120% in cockroaches, and the energy from growth was channeled to compensate for the reduction in metabolism; but, the fraction of assimilated energy allocated to growth was only reduced by 14% in hornworms. These results suggest that, compared to hornworms, cockroaches prioritize metabolism over growth.

The physiological mechanism underlying the well-established negative correlation between Gompertz postnatal growth constant and lifespan across mammalian species remains unclear. For the first time, this study shows that the energetic cost of biosynthesis plays a key role in this correlation. Previously, this cost has been thought to be a constant across species, and therefore was not considered a contributor to the variation in any life history traits. Here, we employ a newly proposed model to explain the physiological effect of the variation in this energetic cost on aging, and how it links growth and lifespan. The conventional life history theory suggested a tradeoff between growth and health of animals, but the new findings here suggest that allocating more energy to biosynthesis may reduce the energetic requirement of somatic maintenance and extend lifespan, and therefore they reveal a more complex nature of the tradeoff.

The energy requirement for biosynthesis plays an important role in an organism’s life history, as it determines growth rate, and tradeoffs with the investment in somatic maintenance. This energetic trait is different between painted lady (Vanessa cardui) and Turkestan cockroach (Blatta lateralis) due to the different life histories. Butterfly caterpillars (holometabolous) grow 30-fold faster, and the energy cost of biosynthesis is 20 times cheaper, compared to cockroach nymphs (hemimetabolous). We hypothesize that physiologically the difference in the energy cost is partially attributed to the differences in protein retention and turnover rate: Species with higher energy cost may have a lower tolerance to errors in newly synthesized protein. Newly synthesized proteins with errors are quickly unfolded and refolded, and/or degraded and resynthesized via the proteasomal system. Thus, much protein output may be given over to replacement of the degraded new proteins, so the overall energy cost on biosynthesis is high. Consequently, the species with a higher energy cost for biosyntheses has better proteostasis and cellular resistance to stress. Our study found that, compared to painted lady caterpillars, the midgut tissue of cockroach nymphs has better cellular viability under oxidative stresses, higher activities of proteasome 20S, and a higher RNA/growth ratio, supporting our hypothesis. This comparative study offers a departure point for better understanding life history tradeoffs between somatic maintenance and biosynthesis.