Principles of seed banks and the emergence of complexity from dormancy

Abstract

Across the tree of life, populations have evolved the capacity to contend with suboptimal conditions by engaging in dormancy, whereby individuals enter a reversible state of reduced metabolic activity. The resulting seed banks are complex, storing information and imparting memory that gives rise to multi-scale structures and networks spanning collections of cells to entire ecosystems. We outline the fundamental attributes and emergent phenomena associated with dormancy and seed banks, with the vision for a unifying and mathematically based framework that can address problems in the life sciences, ranging from global change to cancer biology.

Fig. 1. Seed banks develop among diverse taxa with different life histories and reproductive modes.

A Annual plants, like Lunaria, produce seeds at the end of a growing season, which are deposited into the soil. A well-recognized example of bet-hedging, some fraction of these seeds will delay germination despite optimal conditions. B Daphnia is a planktonic crustacean with parthenogenic reproduction, where females generate offspring without fertilization. When stressed, some species produce males, who in turn fertilize females, leading to the production of dormant resting stages (ephippia) that can persist for extended periods of time in aquatic sediments. C Among many groups of microorganisms, including gut bacteria like Bacteroides, individuals can enter and exit from a dormant state independent of reproduction and without the need of generating physical resting structures. Part (A) image is courtesy of P. Meyer. Part (B) image is courtesy of J. Haney and the illustration is courtesy of J. Ferguson (https://www.paintingbiology.com). Part (C) image is courtesy of C. Skilbeck, (www.cronodon.com).

Fig. 2. Primary attributes (boxes) and transitions (arrows) in a generalized seed-bank model.

In this example, the sizes of the active and dormant pools are made up of an equal number of individuals (N = 70) belonging to different classes (colored squares), which may represent genotypes within a population or species within a community. In the active pool, individuals can be gained through reproduction and lost through mortality. In the dormant pool, there is no reproduction, and mortality of inactive individuals is typically assumed to be much lower than for active individuals, which is reasonable for many but not all taxa that invest in long-lived seed banks. In addition, pool sizes are influenced by stochastic or deterministic transitions between metabolic states (i.e., initiation and resuscitation), which determine the size and rate at which pools undergo turnover. In terms of $\alpha$-diversity, the richness of classes in the dormant pool ($S_d$ = 9) is greater than the richness in the active pool ($S_a$ = 4). In terms of $\beta$-diversity, the active and inactive pools are 82 % dissimilar based on the abundance-weighted Bray-Curtis metric: ${\sum }_{k=1}^S\left[x_{ak}-x_{dk}\right]/{\sum }_{k=1}^S\left(x_{ak}+x_{dk}\right)$, where $x_{ak}$ and $x_{dk}$ correspond to the abundance of class $k$ in the active ($a$) and dormant ($d$) pools, respectively, and $S$ is the number of classes contained in the pools. Seed-bank attributes can also be influenced by migration, especially when dormancy facilitates the dispersal and colonization of individuals in a regional landscape.