Skip to main content
Dryad logo

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

Citation

Bernard, Connor; Compagnoni, Aldo; Salguero-Gómez, Roberto (2019), Testing Finch’s hypothesis: the role of organismal modularity on the escape from actuarial senescence, Dryad, Dataset, https://doi.org/10.5061/dryad.7pvmcvdpk

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 hypothesised three decades ago that species with the ability to compartmentalise risk may escape senescence. Here, we first revew 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 open-access databases to comparatively analyse various moments of senescence and link longevity to the degree of anatomic 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 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.

Methods

This dataset is based on an index for animal anatomies that reflects the subdivisionality/multiplicity of organs. The dataset was compiled to analyse proxies of anatomic redundancy in unitary animals - described in the linked manuscript. The authors of this data relied on a combination of review articles and textbooks to identify anatomical configurations (detailed below). The scope of the data is limited to renal anatomy and the lymphatic system; limitations of this dataset are described in the linked manuscript. The two physiological systems selected for this dataset were prioritized over other physiological systems because a higher-level review showed high variation in the degree to which organs in these systems comprise multiple constituent sub-parts (in contrast to cardiological systems/respiratory systems/digestive systems/etc.). There is opportunity to develop this framework for broader physiological applications; to the best of the author's knowledge, this is a pioneering effort at applying of subdivision index across a broad taxanomic groups. Because this dataset is an early construction, it should be approached with caution. Data will be updated/corrected if more current information is identified, or if any data infelicities are discovered. Detailed notes on changes to this dataset will be annotated. Please contact the corresponding author with any questions/discoveries of error. More detailed methods and information about the determinations on categories (see usage notes) can be found in the manuscript.

--

Data on lymph anatomy is based principally on: Cooper, E., 2019. Advances in Comparative Immunology. Springer.

Cross-validation and additional, detailed information was provided by:

  • Budras, K.D., Hullinger, R.L. and Rautenfeld, D.B.V., 1987. Lymph heart musculature in birds. Journal of morphology191(1), pp.77-87.
  • Boehm, T., Hess, I. and Swann, J.B., 2012. Evolution of lymphoid tissues. Trends in immunology33(6), pp.315-321.
  • Chiba, A., Torroba, M., Honma, Y. and Zapata, A.G., 1988. Occurrence of lymphohaemopoietic tissue in the meninges of the stingray Dasyatis akajei (Elasmobranchii, Chondricthyes). American journal of anatomy183(3), pp.268-276.
  • Owens, L., 2010. Insight into the lymphoid organ of penaeid prawns: a review. Fish & shellfish immunology29(3), pp.367-377.

-

Data on Renal Anatomy based principally on: Bentley, P.J. (1971). Endocrines and Osmoregulation: A Comparative Account in Vertebrates. Heidelberg, Germany: Springer.

Cross-validation and additional, detailed information was provided by:

  • Yokota, E., Kawashima, T., Ohkubo, F., & Sasaki, H. (2008). 1348 Comparative anatomical study of the kidney position in amniotes using the origin of the renal artery as a landmark. Okajimas Folia Anatomica Japonica, 81(6), 135–142. doi: 10.2535/ofaj.81.135
  • Williams, T.M., & Worthy, G. (2009). Anatomy and physiology: the challenge of aquatic living. In Marine Mammal Biology: An Evolutionary Approach. Wiley. Hoelzel, A.R. (Ed.). Hoboken, New Jersey, USA.
  • Ortiz, R.M., 2001. Osmoregulation in marine mammals. Journal of Experimental Biology204(11), pp.1831-1844.
  • Beuchat, C.A., 1999. Kidney structure of a euryhaline mammal, the Cape clawless otter (Aonyx capensis). African Zoology34(4), pp.163-165.

Usage Notes

The levels/factors in the dataset are structured as follows:

Rank Order Factors: Immune Anatomy/Lymphatic Organs

#1 - Lymph Nodes

#2 - Lymph Hearts

#3 - Miscelaneous multi-constituent lymph tissues

#4 - Spleen with no lymph peripherals

#5 - No centralized immune anatomy

--

Rank Order Factors: Osmoregulatory Organs

#1 - Reniculated Kidneys

#2 - Kidneys + Salt Glands or Kidneys + Gills

#3 - Kidney(s)

#4 - Protonephros/Mesonephros

#5 - Other/None