Selection for small body size favours contrasting sex-specific life histories, boldness and feeding in medaka, Oryzias latipes

Abstract

Background Studying variation in life-history traits and correlated behaviours, such as boldness and foraging (i.e., pace-of-life syndrome), allows us to better understand how these traits evolve in a changing environment. In fish, it is particularly relevant studying the interplay of resource abundance and size-selection. These are two environmental stressors affecting fish in natural conditions, but also associated with human-induced environmental change. For instance, fishing, one of the most important threats for freshwater and marine populations, results in both higher mortality on large-sized fish and reduced population density. Results Medaka, Oryzias latipes, from lines selected for large or small size over ten generations, were exposed individually to high or low food availability from birth to adulthood. Maturation schedules, reproductive investment, growth, boldness and feeding were assessed to evaluate the effect of size-selection on the pace of life, and whether it differed between food contexts (high and low). Different food abundance and size-selection resulted in diverse life histories associated with different feeding and boldness behaviour, thus showing different pace-of-life-syndromes. High availability of food favoured faster growth, earlier maturation and increased shyness. Selection for small size led to slower growth in both males and females. But, the life-history trajectory to reach such growth was sex- and food-specific. Under low food conditions, females selected for small size showed earlier maturation, which led to slower adult growth and subsequent low willingness to feed, compared to females selected for large size. No line differences were found in females at high food conditions. In contrast, males exposed to selection for small size grew slower both as juvenile and adult, and were bolder under both feeding regimes. Therefore, the response to size-selection was more sensitive to food availability in females than in males. Conclusions We showed that size-selection (over ten generations) and resource abundance (over developmental time) led to changes in life history and behaviour. However, the effect of size-selection was sex- and context-specific, calling for precaution when drawing general conclusions on the population-level effects (or lack of them) of size-selective fishing. Conservation and management plans should consider this sex- and context-specificity. Electronic supplementary material The online version of this article (10.1186/s12862-019-1460-x) contains supplementary material, which is available to authorized users.

Ecological ramifications of adaptation to size-selective mortality

“…8: 210842 rates of LB medaka. This suggests that SB medaka have reduced willingness to forage on benthos, as seen in earlier studies (silverside Menidia menidia: [28], medaka: [27]). We speculate that LB fish are more efficient foragers within the bottom substrate, where small and cryptic prey such as Nematoda and Ostracoda are difficult to find.…”

Unidirectional response to bidirectional selection on body size II Quantitative genetics

“…explain the lower-than-expected body-size response to selection. However, this possibility is dismissed by indirect evidence from an independent phenotyping experiment in which fish from the present selection experiment at later generations were raised in individual tanks (Diaz-Pauli et al, 2019). In absence of competition, the genetic difference between the Large and Small lines was not larger than we found here, indicating that removing competition did not magnify the phenotypic effects of selection on medaka body size.…”

Unidirectional response to bidirectional selection on body size II. Quantitative genetics

“…Virtually all the phenotypic difference was built in two generations of selection, and there was no more phenotypic progress from generations F 3 to F 6 . The difference between Large and Control lines dropped to less than 1 mm in the last generation, but indirect evidence suggest that this was not a stable genetic effect (e.g., the phenotypic difference between Large and Small lines was maintained in fish from later generations, Diaz‐Pauli, Garric, Evangelista, Vøllestad, and Edeline (2019). Surprisingly, there was no significant difference between the Control and the Small line; that is, the Small line did not respond to selection on size.…”

“…This mechanism could have biased the selection response estimates, and explain the lower‐than‐expected body size response to selection. However, this possibility is dismissed by indirect evidence from an independent phenotyping experiment in which fish from the present selection experiment at later generations were raised in individual tanks (Diaz‐Pauli et al., 2019). In absence of competition, the genetic difference between the Large and Small lines was not larger than we found here, indicating that removing competition did not magnify the phenotypic effects of selection on medaka body size.…”