Aged virgin adults respond to extreme heat events with phenotypic plasticity in an invasive species, Drosophila suzukii

Highlights

• Mating may alter heat tolerance, its plasticity and their decline rate during aging.

• Mated and virgin adults may take different strategies to cope with heat stress.

• Rise of basal heat tolerance may benefit mated females to buffer heat stress.

• Plasticity of heat tolerance may benefit virgin adults to buffer heat stress.

• Mating status of adults should be consider in invasive risk assessment.

Abstract

Climate warming has increased the frequency of extreme heat events. Alien species usually invade new areas with a low-density population and often have limited mating opportunities due to the unsynchronized emergence of adults. Early-emerging virgin adults often have to wait to mate with later-emerging partners at the cost of aging, which reduces thermal tolerance. To understand the adaptive strategies of virgin males/females versus those of mated males/females in response to heat stress during aging, we conducted a fully factorial experiment to test the basal and plastic heat tolerance (CTmax, critical thermal maximum) of males and females with different mating statuses (virgin and mated) at different ages (5, 10, and 15 days after eclosion) after different acclimation regimes (null, rapid and developmental heat acclimation) in a well-known invasive species, Drosophila suzukii. We found that mating could change the heat tolerance of adults during aging. Mated females had higher basal heat tolerance than virgin females, while mated males had lower tolerance than virgin males. Mating could generally decrease the acclimation capacity (i.e., plasticity of heat tolerance) during aging. Aged virgin adults had a much higher acclimation capacity than aged mated adults. Our findings suggest that phenotypic plasticity of heat tolerance may be a main strategy used by virgin adults to cope with heat events. The phenotypic plasticity of thermal tolerance could increase the invasion success of alien species in new areas by allowing them to rapid respond to local temperature changes.

Introduction

Climate warming increases the frequency and success of invasion events because it can bring about the expansion of species distributions into high-latitude or -altitude regions, reducing the competitive advantages of native species over invasive species (Dukes and Mooney, 1999, Walther et al., 2009, Diez et al., 2012). Overwintering may be a key factor influencing the population establishment of invasive species in new areas (Leather et al., 1995, McDonald et al., 2000). However, population increases (Ma et al., 2015a, Ma et al., 2015b) and successful expansion (Battisti et al., 2006, Pateman et al., 2012) could be strongly influenced by summer temperatures. Climate warming has increased the frequency and intensity of extreme heat events (Rahmstorf and Coumou, 2011, IPCC, 2014), which may greatly reduce the thermal safety margin of organisms (Deutsch et al., 2008, Paaijmans et al., 2013). Thus, the ability to buffer extreme high temperatures in summer becomes critical for successful invasion. Organisms have evolved adaptive mechanisms to buffer heat stress (Hoffmann et al., 2003, Xue et al., 2019). Phenotypic plasticity in heat tolerance improves fitness through rapid and flexible responses to temperature changes (Chown and Terblanche, 2006, Sgrò et al., 2016) without changing gene sequences/frequencies (Schlichting and Pigliucci, 1993, Schlichting and Wund, 2014). This plasticity is beneficial for invasive species to survive under extreme temperature conditions by increasing their upper thermal limits (Angilletta, 2009, Colinet and Hoffmann, 2012, Sgrò et al., 2016, Seebacher et al., 2015), which may increase their invasion success (Chown et al., 2007, Nyamukondiwa et al., 2010, Shearer et al., 2016). Therefore, a better understanding of heat tolerance and its plasticity is of great importance in the prediction of invasion risk under climate warming.

Successful copulation and reproduction are essential for alien species to establish and increase populations in new areas (Liebhold and Tobin, 2008). Adults differing in mating status may have different energy allocation strategies (Trivers, 1972, Alexander and Borgia, 1979). Females and males play different roles in reproduction. Successfully copulated females allocate more energy to reproduction, while mated males are not important in reproduction. However, virgin females or males might spend their time and energy finding suitable heterosexual individuals with which to copulate, especially when the initial population remains at a low density at the beginning of colonization and the males and females do not emerge simultaneously (Trivers, 1972, Alexander and Borgia, 1979, Slansky, 1980, Simmons et al., 1992). Thus, early-emerging virgin males or females must pay the cost of aging while waiting for copulation. Importantly, aging can significantly reduce basal thermal tolerance (Bowler, 1967, Davison, 1969, Bowler and Terblanche, 2008, Colinet et al., 2013, Chidawanyika et al., 2017) and plastic heat tolerance (Sørensen and Loeschcke, 2002, Jensen et al., 2007, Pappas et al., 2007).

If extreme heat events occur during adult aging, two questions emerge: 1) Do virgin adults respond to extreme temperatures differently from mated adults during aging, and what is the potential function of such differences? 2) Do mated/virgin females respond to extreme high temperatures differently than mated/virgin males during aging, and what are the potential biological functions? Based on our literature survey, the impact of mating on heat tolerance during aging has not been studied in detail, although mating can weaken the cold tolerance of adults in Ophraella communa (Zhao et al., 2019) and Harmonia axyridis (Facon et al., 2017). Mating could benefit females in toleration of starvation and desiccation. Mated females are more tolerant than virgin females to starvation stress in Drosophila melanogaster (Service, 1989, Rush et al., 2007, Goenaga et al., 2012), and desiccation in two desert Drosophila (Drosophila mojavensis and Drosophila arizonae) (Knowles et al., 2004, Knowles et al., 2005). Previous studies have mainly focused on the impact of mating on basal stress tolerance, while the impact of mating on acclimation capacity (i.e., phenotypic plasticity of stress tolerance) has not been directly investigated clearly.

We selected spotted wing drosophila (SWD), Drosophila suzukii Matsumura (Diptera: Drosophilidae), a widely investigated invasive species in recent years (Asplen et al., 2015), as our model system. SWD is native to Asia and was first described by Matsumara in 1931 (Bächli, 2015). It has thus far successfully colonized the Americas and Europe (Kanzawa, 1939, Cini et al., 2012, Asplen et al., 2015). In contrast to Drosophila melanogaster, SWD has caused severe economic damage in invaded countries because it has a serrated ovipositor and exclusively lays eggs inside many preharvest or ripe soft-skinned fruits, such as berries, cherries, and grapes (Walsh et al., 2011, Karageorgi et al., 2017). Thus, potential invasion risk assessment of SWD based on basal and plastic thermal tolerance has become important (Valladares et al., 2014, Langille et al., 2017, dos Santos et al., 2017). The cold tolerance of SWD adults in the overwintering stage has been intensively investigated (Enriquez and Colinet, 2017, Ryan et al., 2016, Jakobs et al., 2015, Wallingford and Loeb, 2016), and used to assess the invasion risk (Jakobs et al., 2015, Kaçar et al., 2015, Plantamp et al., 2016, Tonina et al., 2016). However, the heat tolerance of SWD has not been largely investigated. A better understanding of heat tolerance and its phenotypic plasticity during aging will be helpful in invasion risk assessment under climate change.

Here, we measured the basal and plastic heat tolerance (CTmax) of SWD male and female adults with different mating statuses (mated and virgin) and ages (5, 10, and 15 days). Furthermore, we calculated the acclimation capacity i.e., phenotypic plasticity of heat tolerance, based on the method of Kellett et al. (2005). We aimed to clarify whether virgin males and females waiting for copulation have different stress tolerance strategies than successfully mated adults during aging and the biological significance of such strategies. Our results indicate that mating could change the heat tolerance of adults during aging. Mated females had higher basal heat tolerance than virgin females, while mated males had lower tolerance than virgin males. Mating could also generally decrease acclimation capacity. Aged virgin adults had a much stronger acclimation capacity than aged mated adults. Phenotypic plasticity may be a beneficial approach for virgin adults to adapt to extreme temperature conditions during aging, which would help adults of alien species increase the probability of successful copulation and reproduction.