Pace of life syndrome under warming and pollution: integrating life history, behavior, and physiology across latitudes

Abstract

To fully comprehend and predict the impact of drivers of global change such as climate warming and pollution, integrated multi‐trait approaches are needed. As organismal traits are often correlated, responses to stressors are expected to induce coordinated changes in many traits. A promising framework to study this is the pace of life syndrome (POLS), which predicts the integration of life history, behavioral, and physiological traits along a fast‐slow continuum. Using an integrative multi‐trait approach, we evaluated the presence of a POLS both within and across latitudes and how POLS patterns are affected by warming and metal pollution. We studied this in Ischnura elegans damselfly larvae of replicated low‐ and high‐latitude populations that strongly differ in voltinism (three to four generations per year vs. one generation every two years) reared in a common‐garden experiment at two temperatures. Across latitudes, life history, behavior, and physiology covaried in accordance with the POLS, with the fast‐paced low‐latitude damselflies characterized by a fast growth rate, high activity, and more explorative and risk‐taking behavior, fast metabolic rate, and low investment in immune function (activity of phenoloxidase). This fast POLS strategy was associated with a higher sensitivity to metal exposure and a higher vulnerability to predation. Warming caused opposite responses between the latitudes consistent with differential thermal adaptation in growth rate, behavior, and oxidative stress parameters. Despite this, damselflies of both latitudes showed a consistent pattern in phenotypic correlations among traits that, moreover, was not affected by warming and metal exposure. Within latitudes, there was no full support for the POLS. More active larvae were more explorative and risk taking, which aligned with the fast‐slow life history axis, but less strong than at the across‐latitude level. Physiological traits were also integrated within latitudes, yet there was no unambiguous coupling with the fast‐slow life history continuum. The consistent syndrome structure, if underpinned by genetic correlations, may restrict the independent evolution of individual traits, yet may not necessarily constrain adaptive evolution of integrated trait sets. This is because the covariance pattern was to a large extent similar across latitudes and within latitudes, suggesting adaptive trait integration guiding adaptive evolution of trait sets along the fast‐slow continuum.

Live fast, die old: oxidative stress as a potential mediator of an unexpected life‐history evolution

“…The study species shows striking latitudinal differences in life history, with higher larval growth rates in the multivoltine (3–4 generations per year), low‐latitude populations compared to the semivoltine (2 years per generation), high‐latitude populations (Stoks and De Block , Shama et al , Stoks et al , Debecker et al , Debecker and Stoks , Van Dievel et al , Verheyen and Stoks ). Moreover, we have recently shown in separate studies that the low‐latitude populations of the species have a longer adult lifespan (reported as Supporting Information in Debecker et al ) and higher levels of antioxidant enzymes in the larval stage (Debecker and Stoks ). Building on these previous findings, the current study aims to elucidate the mechanism underpinning this atypical fast growth – long lifespan pattern in terms of oxidative stress physiology.…”

“…Mated females were collected in the field from two populations in southern Sweden (Genarp 55°36′N, 13°23′E and Vallby 55°38′N, 13°17′E) where the species is semivoltine, and from two populations in southern France (St‐Martin De Crau 43°37′N, 4°46′E and Salin de Giraud 43°24′N, 4°43′E) where the species has 3–4 generations per year (Corbet et al ). Ponds in these regions do not show latitudinal differentiation in several abiotic (pH, oxygen levels) and biotic variables (chlorophyll a levels, densities of fish and macroinvertebrate predators) (Debecker and Stoks ). Mean summer water temperatures in these ponds are ~24°C in southern France and ~20°C in southern Sweden (Debecker and Stoks ).…”

“…faster growth and development rates), but also suffer a higher vulnerability to oxidative stress and a shorter lifespan (Ricklefs and Wikelski , Réale et al ). Recent work in this field indeed identified oxidative stress physiology as part of this syndrome (Arnold et al , Brans et al , Debecker and Stoks ). Yet, studies explicitly testing for oxidative‐stress mediated costs of a rapid growth in terms of a reduced lifespan are missing (but see Vágási et al for evidence at the species level, and Meniri et al for short‐term survival costs).…”

“…Although evidence for costs of rapid growth working through oxidative damage has been accumulating in recent years (Nussey et al , Noguera et al , Geiger et al , Christensen et al , Smith et al , Kim et al , Burraco et al 2020), these studies did not consider multiple populations across latitudes (but see Debecker and Stoks ), and none looked at effects on lifespan. Hence, it is unknown whether oxidative stress‐mediated costs of rapid growth play a mediatory role in the differential evolution of growth rates and lifespan at high and low latitudes.…”

Environmental unpredictability shapes glucocorticoid regulation across populations of tree swallows

“…Global environmental changes are altering the habitats of many species (Peñuelas et al, 2013). For 30 species with wide geographic ranges, intra-specific variation in life-history strategies resulting from 31 historical selection might predispose some populations to be more or less susceptible to increasing 32 environmental changes (Candolin, 2019;Debecker and Stoks, 2019;Harding et al, 2019). Environmental 33 variation favors individuals that differentially allocate time and energy to reproduction and self-34 maintenance in order to maximize lifetime fitness (Stearns, 1989;Stearns, 1992;Ricklefs and Wikelski, 35 2002).…”