Decades of warming alters maturation and reproductive investment in fish

Abstract

How does warming affect maturation and reproductive investment in ectotherms? Younger age and smaller size at maturation, as well as altered reproduction processes, have been found in a few species subjected to elevated temperatures. These observations, however, come from studies that do not distinguish effects of warming on maturation from those on growth, are also restricted to single generation responses to warming, or have additional stressors besides warming in the study system. Here, we study warming effects on maturation and reproductive investment in wild, unexploited fish populations using a whole‐ecosystem heating experiment. The experiment is conducted on Eurasian perch (Perca fluviatilis) in a heated and control area (with >5°C temperature difference) in the Baltic Sea. We compare female perch size at maturation using estimated probabilistic maturation reaction norms (PMRNs) and the gonado‐somatic index over 17 years of heating, spanning approximately five to eight perch generations. Using the PMRN approach, we show that warming has substantial effects on maturation size independent of warming‐induced changes in body growth. We found that young fish mature at a smaller size and invest more in developing their gonads in the heated population than in the unheated population. Our findings suggest that warming effects on reproductive investment may initially compensate for the cost of warming‐induced decrease in maturation size caused by the trade‐off between early maturation and size‐dependent fecundity. After multiple additional generations of warming, maturation and reproduction traits in perch differed from those in the first generations following the onset of warming, which suggests that warming‐induced evolution may have occurred. Our study is particularly relevant in the context of climate change because of the unusually large temperature difference between the areas and the fact that the heating occurred on an ecosystem level. We call for experimental studies resolving mechanisms of trait responses to warming across generations, complemented with genomic analyses, to aid understanding of organisms' long‐term responses to climate change.

Larger but younger fish when growth outpaces mortality in heated ecosystem

“…Both patterns have been used to explain how growth can increase for small and young fish, while large and old fish typically do not benefit from warming. Our study species is no exception to these rules ( Huss et al, 2019 ; Karås and Thoresson, 1992 ; Niu et al, 2023 ; Sandstrom et al, 1995 ). This suggests that growth dynamics under food satiation may not be directly proportional to those under natural feeding conditions ( Railsback, 2022 ).…”

“…The contrasts lie in that both asymptotic size and size-at-age of mature individuals, as well as the proportion of larger individuals, were slightly larger and higher in the heated area—despite the elevated mortality rates. This result was unexpected for two reasons: optimum growth temperatures generally decline with body size within species under food satiation in experimental studies ( Lindmark et al, 2022 ), and fish tend to mature at smaller body sizes and allocate more energy into reproduction as it gets warmer ( Niu et al, 2023 ; Wootton et al, 2022 ). Both patterns have been used to explain how growth can increase for small and young fish, while large and old fish typically do not benefit from warming.…”

Unlocking the genome of perch – From genes to ecology and back again

“…Without genetic evidence, these methods can potentially indicate but not demonstrate evolution. They were originally used to study fisheries‐induced evolution (Dieckmann & Heino, 2007; Swain et al, 2007), but have recently been applied also to trait responses to warming (Crozier et al, 2011; Niu et al, 2023). For example, perch in a multi‐generational heating experiment in the wild mature at a smaller size than perch in the control site with natural temperatures (Niu et al, 2023).…”

“…They were originally used to study fisheries‐induced evolution (Dieckmann & Heino, 2007; Swain et al, 2007), but have recently been applied also to trait responses to warming (Crozier et al, 2011; Niu et al, 2023). For example, perch in a multi‐generational heating experiment in the wild mature at a smaller size than perch in the control site with natural temperatures (Niu et al, 2023). High‐throughput sequencing allows us to combine these findings on trait changes with analyses of genetic variation among individuals from both the heated and the control population at multiple time points throughout the 40‐year heating experiment (Niu et al, 2023).…”

Fish life histories in a warming climate: a mechanistic basis of change and a community context

“…It is becoming increasingly evident that higher energy allocation to reproduction at the cost of growth is a likely response to increasing temperature (Loisel et al 2019;Fryxell et al 2020;Wootton et al 2022;Niu et al 2023). However, we do not know what temperature driven energetic changes, what demographic processes and species-specific ecology drives selection on energy allocation strategies in response to warming.…”