Testing Finch's hypothesis: The role of organismal modularity on the escape from actuarial senescence

Abstract

1. Until recently, senescence was assumed to be a universal phenomenon. Evolutionary theories of senescence predict that no organism may escape the physiological decline that results in an increase in mortality risk and/or decline in fertility with age. However, evidence both in animals and plants has emerged in the last decade defying such predictions. Researchers are currently seeking mechanistic explanations for the observed variation in ageing trajectories. 2. We argue that the historical view on the inevitability of senescence is due, in part, to the development of its classical theories, which targeted primarily unitary organisms. In unitary species, the integration of resources and functions is high, and adult size is determined. In contrast, the architecture of modular organisms is indeterminate and built upon repeated modules. The isolation of mortality risk in species like hydra (Hydra spp.) or creosote brush Larrea tridentata may explain their null or even negative senescence. 3. Caleb Finch hypothesized three decades ago that species with the ability to compartmentalize risk may escape senescence. Here, we first review the evidence on organisms that slow down or even avoid senescence in the context of their architecture, along a continuum of unitarity-modularity. Then, we use openaccess databases to comparatively analyse various moments of senescence and link longevity to the degree of anatomical modularity. Our analysis compares the pace of senescence across 138 plants and 151 animals, and the shape of senescence across a subset of these. Our comparative analysis reveals that plant species that are more modular do indeed tend to escape from senescence more often than those that are unitary. The role of modularity in animal senescence is less clear. 4. In light of novel support for Finch's hypothesis across a large diversity of plant species, and with less conclusive findings in animals, we identify new research directions. We highlight the opportunities related to age-dependent mortality factors. Other areas for further research include the role of modularity in relation to endocrine actions, and the costs of modular anatomies.

On tree longevity

“…Diploxylon Mediterranean pine that evolved during the early Tertiary and is now found in highelevation environments, which limit growth and also represent Quaternary refugia (Schirone et al, 1991 (Bernard et al, 2020). Plants of great longevity are characterized by a greater degree of modularity, which is apparent in root-to-shoot connections (Larson et al, 1993), bark stripping, and defense systems that compartmentalize injuries and biotic attackers (Morris et al, 2019).…”

An integrative view of senescence in nature

“…Lucas and Keller (2020) highlight the complex interplay between the evolution of sociality and lifespan, review the research on this topic performed at both interand intraspecific levels and then identify knowledge gaps in our current understanding of these relationships. Finally, Bernard, Compagnoni, and Salguero-Gómez (2020) provide the first general test of Finch's hypothesis that higher modularity should be associated with weaker senescence and find support for this hypothesis in plants, but not in animals.…”

“…This sampling bias is likely explained by the fact that most long-term field studies focused on these species (Clutton-Brock & Sheldon, 2010). The time has now come to expend the range of species where senescence is traditionally investigated in the wild to unravel its diversity (Bernard et al, 2020;Conde et al, 2019;Jones et al, 2014). This special feature puts forward three taxa that are, in that context, full of promise: insects, reptiles and plants.…”

“…Future studies in non-conventional biological models of ageing have the potential to bring new insights on the ecological and biological factors shaping this unappreciated diversity of senescence patterns (Bernard et al, 2020;Hoekstra et al, 2020;Roach & Smith, 2020;Zajitschek et al, 2020). In plants, dormancy is likely to play a key role.…”

“…While the direction of the relationship between the degree of modularity and measures of pace and shape (see Section 2) are in the predicted direction in plants, the picture appears much less clear in animals, which is likely due to a lack of data to assess age dependence from published population projection matrices but also to the difficulty of ranking animals along a modularity continuum. Bernard et al (2020) have notably ranked species according to the degree of modularity of the renal system. However, species with more modular systems (i.e.…”