Integrative biology of injury in animals

Abstract

Mechanical injury is a prevalent challenge in the lives of animals with myriad potential consequences for organisms, including reduced fitness and death. Research on animal injury has focused on many aspects, including the frequency and severity of wounding in wild populations, the short‐ and long‐term consequences of injury at different biological scales, and the variation in the response to injury within or among individuals, species, ontogenies, and environmental contexts. However, relevant research is scattered across diverse biological subdisciplines, and the study of the effects of injury has lacked synthesis and coherence. Furthermore, the depth of knowledge across injury biology is highly uneven in terms of scope and taxonomic coverage: much injury research is biomedical in focus, using mammalian model systems and investigating cellular and molecular processes, while research at organismal and higher scales, research that is explicitly comparative, and research on invertebrate and non‐mammalian vertebrate species is less common and often less well integrated into the core body of knowledge about injury. The current state of injury research presents an opportunity to unify conceptually work focusing on a range of relevant questions, to synthesize progress to date, and to identify fruitful avenues for future research. The central aim of this review is to synthesize research concerning the broad range of effects of mechanical injury in animals. We organize reviewed work by four broad and loosely defined levels of biological organization: molecular and cellular effects, physiological and organismal effects, behavioural effects, and ecological and evolutionary effects of injury. Throughout, we highlight the diversity of injury consequences within and among taxonomic groups while emphasizing the gaps in taxonomic coverage, causal understanding, and biological endpoints considered. We additionally discuss the importance of integrating knowledge within and across biological levels, including how initial, localized responses to injury can lead to long‐term consequences at the scale of the individual animal and beyond. We also suggest important avenues for future injury biology research, including distinguishing better between related yet distinct injury phenomena, expanding the subjects of injury research to include a greater variety of species, and testing how intrinsic and extrinsic conditions affect the scope and sensitivity of injury responses. It is our hope that this review will not only strengthen understanding of animal injury but will contribute to building a foundation for a more cohesive field of ‘injury biology’.

The cost and payout of age on germline regeneration and sexual maturation inPlatynereis dumerilii

“…While there have been anecdotal notes on P. dumerilii’ s ability to regenerate its germline during posterior regeneration (Hauenschild and Fischer, 1969; Rebscher, 2014), systematic studies on this process to see whether removal and regeneration of germ cells have an impact on fertility and fecundity have not been carried out before. In some annelids injury can negatively impact reproduction, measured by the production of gametes, or gamete, cocoon, and brood numbers (Gibbs, 1968; Hill et al, 1982; Rennolds and Bely, 2023; Zajac, 1985). To address this in P. dumerilii , we implemented the most severe survivable amputation at three different developmental stages with differential germline investment states.…”

“…Injury is generally expected to have an energetic cost and consequently a negative effect on growth and reproduction outputs such as reduced fecundity, lower egg numbers, smaller egg size, or longer time to sexual maturation (Olive and Clark, 1978; Rennolds and Bely, 2023). Regenerating sponges and corals may have reduced fecundity or may remain infertile (Henry and Hart, 2005) due to resource trade-offs between regeneration and sexual reproduction.…”

A general framework for modelling trade‐offs in adaptive behaviour

“…impaired immune system, degenerative cell destruction) than merely depleted energy reserves. Following a mechanical injury, reproduction is commonly reduced in favour of regeneration in a wide range of species (Rennolds & Bely, 2023). Accounting for a trade-off between damage and reproduction can dramatically change the predictions of life-history models: using this approach, showed that the classical prediction that organisms should invest increasingly in reproduction as they approach the end of their life (e.g.…”

Investment in regeneration versus asexual reproduction is resource‐dependent in a freshwater annelid

“…These two traits often co‐occur in soft‐bodied taxa like cnidarians, planarians, and annelids (Berrill, 1952; Brockes & Kumar, 2008; Giangrande & Licciano, 2014; Kostyuchenko & Kozin, 2020; Zattara & Bely, 2016). Given the prevalence of injury in wild populations of these groups (Lindsay, 2010; Rennolds & Bely, 2023), allocation strategies involving regeneration and reproduction (whether sexual or asexual) are ecologically relevant and likely have been shaped strongly by natural selection. Both processes require resource investment, leading to short‐ and possibly long‐term physiological and higher‐order consequences.…”

“…Both processes require resource investment, leading to short‐ and possibly long‐term physiological and higher‐order consequences. The costs of both traumatic loss of a body part and its subsequent regeneration can be wide‐ranging and significant (Bely, 2010; Bernardo & Agosta, 2005; Lawrence, 2010; Maginnis, 2006; Rennolds & Bely, 2023). A considerable amount of research has investigated the effects of injury and regeneration on sexual reproduction.…”