Sex-biased phenotypic plasticity affects sexual dimorphism patterns under changing environmental conditions

Abstract

Sexual dimorphism is almost ubiquitous in animals. A common pattern observed across multiple taxa involves differences in development time (sexual bimaturism) and body size (sexual size dimorphism) between conspecific males and females. Furthermore, a strict association of dimorphism at these traits has been documented in several taxa, where the sex showing shorter development time also has a smaller body size than the other sex. Growth and development are strongly dependent on environmental conditions during individual life-cycle in ectotherms, inducing considerable phenotypic plasticity. However, how phenotypic plasticity affects the association between sexual dimorphism in development time and body size remains unclear. Here, we tracked development time, body size, and body mass throughout the ontogeny of the mosquito Aedes mariae. The larval development of this species is strictly linked to Mediterranean Sea rock-pools, whose highly variable environmental conditions over minimal time frames make this organism-environment system ideal for exploring plasticity-led eco-evolutionary processes. We found differential plasticity between males and females, dissolving the link between dimorphism in development time and body size under increasing temperature and decreasing salinity conditions. These findings contrast with the current hypotheses proposed to explain the origin of the association between sexual bimaturism and sexual size dimorphism, highlighting the condition dependence of sexual dimorphism patterns and the need to consider phenotypic plasticity in future studies on their evolution.

Figure 1

Experimental design. All individuals from the egg to third instar larvae were kept at 26 °C and 50 ‰ salinity. Third instar larvae were randomly placed into developmental treatments, and trait measures started. In the first treatment, individuals were maintained at constant conditions of temperature (26 ±  °C) and salinity (50‰, 50 g/l) throughout the experiment (CC). In the second treatment, individuals were exposed to rising temperature (TC) as follows: third instar larvae were maintained at 29 °C; fourth instar larvae at 31 °C, and pupae at 34 °C. In the third treatment, individuals were exposed to decreasing salinity (SC) from 50‰ to 0‰. Weight and digital pictures were obtained within two hours from the ecdysis.

Figure 2

Phenotypic plasticity in development time. Differences in development time between sexes (red = female, blue = male) in (a) constant temperature and salinity condition, (b) rising temperature condition and (c) decreasing salinity condition. Significance levels: *** = P < 0.001, ** = P < 0.01, * = P < 0.05, ns = P > 0.05. Boxplots show median values (middle line), interquartile range (box) and the range values including some outliers (dots which extend beyond the min and max of the boxplot). For each treatment, L3-L4 is the development time computed from L3 to L4 larval instars; L4-P is the development time from L4 larval instar to pupal stage; P-Ad is the development time from pupal to adult stages; Total means the development time from L3 larval instar to adult stage.

Figure 3

Phenotypic plasticity in larval and pupal weight. Weight differences between sexes (red = female, blue = male) in fourth instar larvae (a) and pupae (b) in constant temperature and salinity condition (CC), rising temperature condition (TC), and decreasing salinity condition (SC). Significance levels: *** = P < 0.001, ** = P < 0.01, * = P < 0.05, ns = P > 0.05. Boxplots show median values (middle line), interquartile range (box) and the range values including some outliers (dots which extend beyond the min and max of the boxplot).

Figure 4

Phenotypic plasticity in larval morphological traits. First and second components of PCA analysis on morphometric measures of fourth instar larvae (a, b). Differences between sexes (red = female, blue = male) in constant temperature and salinity condition (CC), rising temperature condition (TC), and decreasing salinity condition (SC). Significance levels: *** = P < 0.001, ** = P < 0.01, * = P < 0.05, ns = P > 0.05. Boxplots show median values (middle line), interquartile range (box) and the range values including some outliers (dots which extend beyond the min and max of the boxplot).

Figure 5

Phenotypic plasticity in pupal morphological traits. First component of PCA analysis on morphometric measures of pupae in constant temperature and salinity condition (CC), rising temperature condition (TC), and decreasing salinity condition (SC). Significance levels: *** = P < 0.001, ** = P < 0.01, * = P < 0.05, ns = P > 0.05. Boxplots show median values (middle line), interquartile range (box) and the range values including some outliers (dots which extend beyond the min and max of the boxplot).