Multigenerational consequences of aphid size on offspring phenotype and reproduction

Abstract

In many organisms, phenotype and fitness are strongly influenced by both current environmental factors and maternal effects. The low genetic variation, high phenotypic plasticity, and telescoping generations seen in aphids permit us to investigate the relative importance and potential interaction of maternal and current environments on phenotype. Although past studies have identified an influence of maternal host plant on offspring phenotype and reproduction in aphids, few have demonstrated the potential for these maternal effects to also interact with the aphid's current environment. By rearing multiple generations of Aphis nerii (Fonscolombe) (Hemiptera: Aphididae) on their host common milkweed, Asclepias syriaca (L.) (Apocynaceae), we tested the relative influence and interaction of both maternal and current environmental effects of crowding and plant quality on aphid body size and reproduction. Our results indicate that aphid body size increased with current plant quality and decreased with aphid density in both generations, with an additional direct, positive relationship between body size and fecundity. We did not find evidence for adaptive maternal effects, e.g., production of fewer, larger, offspring by stressed mothers. Instead, poor maternal environments constrained aphid body size and reproduction. Importantly, these adverse maternal effects were only seen in offspring where subsequent nymph population growth was allowed to increase unchecked, likely reducing available resources. Our study thus demonstrates that the significance of maternal effects in aphid development and reproduction can depend on current resource availability, shaping the phenotype and fecundity of offspring under stressful conditions. Incorporating this framework for how aphid body size and reproduction respond to current and maternal environments may improve predictions for how aphid population growth is impacted by resource limitation across generations.

Transgenerational plasticity in aphids reared in a poor-resource environment

“…We also showed that a poor maternal environment always constrains the body size, survival, and fecundity of the next generation. This has been reported in previous studies ( Hayden et al, 2021 ; Zehnder et al, 2007 ). However, trans-generational effects on organismal development are related to resource abundance, as parents reared in a resource-limited environment produce offspring of lower quality due to reduced nutrient supply ( Baker et al, 2018 ; Herman and Sultan, 2016 ).…”

“…Under adverse conditions such as starvation ( Scharf, 2016 ), adult Sitobium avenae (Fabricius) aphids showed reduced longevity and fecundity ( Xu et al, 2019 ). Herbivorous insects exhibit a high degree of phenotypic and transgenerational plasticity in their physiological and behavioral responses to changes in host plant quality, which in turn affects how they interact with the plant ( Ashra and Nair, 2022 ; Hayden et al, 2021 ). Important life history traits of aphids, such as body size, survival, developmental rate, and fecundity, are negatively affected by a poor quality of the host plant ( Dixon, 1987 ; Hayden et al, 2021 ; Ríos Martínez and Costamagna, 2018 ) or when the plant is damaged by other herbivores ( Denno et al, 2000 ; Takemoto et al, 2013 ).…”

“…Herbivorous insects exhibit a high degree of phenotypic and transgenerational plasticity in their physiological and behavioral responses to changes in host plant quality, which in turn affects how they interact with the plant ( Ashra and Nair, 2022 ; Hayden et al, 2021 ). Important life history traits of aphids, such as body size, survival, developmental rate, and fecundity, are negatively affected by a poor quality of the host plant ( Dixon, 1987 ; Hayden et al, 2021 ; Ríos Martínez and Costamagna, 2018 ) or when the plant is damaged by other herbivores ( Denno et al, 2000 ; Takemoto et al, 2013 ). The feeding environment is then important in modulating the phenotype of aphids, as these organisms can alter their physiological and morphological traits to adapt to the new current environment.…”

“…For example, body size and fecundity of Aphis gossypii are influenced by the nutritional quality of the host plants, but a stronger effect is due to the quality of the host plant on which the parental generation feeds ( Nevo and Coll, 2001 ). In Aphis nerii (Fonscolombe), variation in some life history traits may depend on current and maternal resource availability, but there is no evidence for adaptive maternal effects ( Hayden et al, 2021 ).…”