Carryover effects of larval environment on individual variation in a facultatively diadromous fish

Abstract

Intraspecific trait variation may result from “carryover effects” of variability of environments experienced at an earlier life stage. This phenomenon is particularly relevant in partially migrating populations composed of individuals with divergent early life histories. While many studies have addressed the causes of partial migration, few have investigated the consequences for between‐individual variability later in life. We studied carryover effects of larval environment in a facultatively diadromous New Zealand fish, Gobiomorphus cotidianus, along an estuarine salinity gradient. We investigated the implications of varying environmental conditions during this critical stage of ontogeny for adult phenotype. We inferred past environmental history of wild‐caught adult fish using otolith microchemistry (Sr/Ca) as a proxy for salinity. We tested for main and interactive effects of larval and adult environment on a suite of traits, including growth rates, behavior (exploration and activity), parasite load, and diet (stable isotopes and gut contents). We found a Sr/Ca consistent with a continuum from freshwater to brackish environments, and with different trajectories from juvenile to adult habitat. Fish with Sr/Ca indicating upstream migration were more vulnerable to trematode infection, suggesting a mismatch to freshwater habitat. Diet analysis suggested an interactive effect of larval and adult environments on trophic position and diet preference, while behavioral traits were unrelated to environment at any life stage. Growth rates did not seem to be affected by past environment. Overall, we show that early life environment can have multiple effects on adult performance and ecology, with the potential for lifetime fitness trade‐offs associated with life history. Our study highlights that even relatively minor variation in rearing conditions may be enough to generate individual variation in natural populations.

Pre‐ to post‐fledging carryover effects and the adaptive significance of variation in wing development for juvenile songbirds

“…The potential for morphological traits to generate carryover effects is of particular interest in juvenile animals, as they face key transitional periods between life stages that are critical with respect to recruitment, life‐history evolution and viability of animal populations (Martin & Briskie, 2009). Examples include dispersal of hatchling turtles (Smith, Steen, Conner, & Rutledge, 2013), metamorphosis in anurans (Van Allen, Briggs, McCoy, & Vonesh, 2010) migration of aquatic vertebrate larva from rearing to adult environments (Saboret & Ingram, 2019) and nest leaving in mammals (Carrier, 1995). The conditions individuals experience pre‐transition may therefore have a large influence on the development of key traits, generating carryover effects which drive subsequent survival and influence variation of animal life histories.…”

No Evidence for Long-Term Carryover Effects in a Wild Salmonid Fish

“…The studies that found longer lasting effects in fish used natural variation in larval traits such as growth rate, condition, or early life environment (e.g. Shima and Swearer, 2010;Saboret and Ingram, 2019), again highlighting that the life stage at which a stressor occurs may be an important factor in determining whether effects carryover to adulthood.…”

“…Many studies have considered the effects of stressors on migrating adult animals (Norris and Taylor, 2006 and references therein;O'Connor et al, 2014 and references therein), but none that we know of have manipulated migratory animals at the juvenile stage that must also overcome some form of physiological transition. Yet there is evidence this may be important, as natural variation in salinity experienced during the larval stage in the facultatively diadromous common bully (Gobiomorphus cotidianus) affects vulnerability to parasites, trophic position, and diet preference in adulthood (Saboret and Ingram, 2019). Species that face a physiological transition while migrating are likely challenged to a greater extent because energy must also be allocated to the physiological processes necessary to deal with this transition, though our current study suggests this is not the case for brown trout.…”

Which factors determine the long‐term effect of poor early‐life nutrition? A meta‐analytic review

“…later in life (Crino and Breuner 2015), such as a tolerance to starvation later in life after being starved in early life (Wang et al 2016). Experiential legacies can thus result in many different possible responses to the early-life environment, which might underlie phenotypic variation among individuals at older life stages (Beckerman et al 2003, Senior et al 2017, Saboret and Ingram 2019. Given the difficulty in tracking individuals throughout their life, however, a full understanding of the impact of early-life conditions on subsequent individual performance and population dynamics is still lacking (but see Beckerman et al 2003).…”

“…2003, Senior et al. 2017, Saboret and Ingram 2019). Given the difficulty in tracking individuals throughout their life, however, a full understanding of the impact of early‐life conditions on subsequent individual performance and population dynamics is still lacking (but see Beckerman et al.…”