1. Introduction

Ecological and evolutionary processes acting during range expansion (Bowler & Benton, 2005; Kokko & López-Sepulcre, 2006; Kubisch et al., 2014) are key to understanding the spread of invasive species (Hastings et al., 2005), potential success of biological control agents (Szűcs et al., 2019), and the ability of threatened species to track recent climate change (Mustin et al., 2009). The landscapes encountered by range expanding populations represent novel selective environments (Brown et al., 2013; Van Petegem et al., 2016), and simultaneously, the expansion itself can be a catalyst for evolution through spatial sorting and founder effects (Phillips et al., 2010b; Shine et al., 2011). Thus, range expansion can result in evolved differences in reproductive life-history and dispersal traits between populations at the core of the range and the edge of the expansion front (Peischl et al., 2013; Phillips, 2015; Simmons & Thomas, 2004).
The effect of range expansion on reproductive life-history traits, such as fecundity and age at first reproduction, depends upon whether selection or non-adaptive evolutionary processes are dominant at the expansion front (Phillips et al., 2010b). Selection is hypothesized to differ between core and edge due to differences in density (Burton et al., 2010; Fronhofer & Altermatt, 2015). Stable, high-density populations at the core generally exhibit density-dependent growth, where selection favors competitive ability (Phillips et al., 2010b). At the expansion front, population densities are low and competition is relaxed, so populations generally exhibit density-independent growth (Altwegg et al., 2013; Burton et al., 2010) and selection favors high fecundity and early reproduction (Fig. 1A, solid arrow) (Brommer et al., 2002; Phillips et al., 2010b). However, edge populations may be so small that genetic drift can overwhelm selection, and deleterious alleles may ‘surf’ the wave of expansion during repeated founder events (Klopfstein et al., 2006). When these non-adaptive processes are dominant, edge populations may experience reduced fitness, or expansion load, relative to the core (Fig. 1A, dashed arrow) (Peischl et al., 2013; Peischl & Excoffier, 2015; Travis et al., 2007). Additionally, fecundity at the edge may be reduced relative to the core due to trade-offs between dispersal, reproduction, and competitive ability (Burton et al., 2010; Fronhofer & Altermatt, 2015; Phillips et al., 2010b).
Range expansion theory predicts that populations at the expanding edge will evolve increased dispersal ability relative to populations at the core through the process of spatial sorting (Phillips et al., 2008; Shine et al., 2011; Travis & Dytham, 2002). Spatial sorting occurs as individuals with greater dispersal ability are more likely to arrive at the range edge and disperse to new territory, resulting in populations at the expanding edge being a non-random selection of better dispersers. Since dispersal ability is heritable in many species (Saastamoinen et al., 2018), this gradient is further reinforced by spatially assortative mating among individuals at the edge. Despite strong evidence for spatial sorting (Berthouly-Salazar et al., 2012; Hill et al., 2011; Lombaert et al., 2014; Merwin, 2019; Monty & Mahy, 2010; e.g. Phillips et al., 2006, 2010a), some factors may inhibit or weaken evolutionary shifts in dispersal between core and edge. For example, adaptation to novel environments could slow expansion speed and reduce spatial selection on dispersal (Andrade-Restrepo et al., 2019; Hillaert et al., 2015). Additionally, species that are unlikely to disperse from low-density patches may be less likely to evolve increased dispersal ability at the edge of the range expansion (Fronhofer, Gut, et al., 2017; Travis & Dytham, 2002).
Dispersal is a multi-faceted behavior that involves individual choices about whether and how far to move. Dispersal may be informed by intraspecific interactions such as the presence of relatives and population density (Bitume et al., 2013; Endriss et al., 2019), and factors internal to the organism such as body condition, sex, or mating status (Fig. 1B) (Clobert et al., 2009; Schumacher et al., 1997). For many species, high population density can signal strong intraspecific competition, which may increase emigration (positive density-dependence) (Altwegg et al., 2013). Alternatively, species for which the benefit of living near conspecifics (e.g. mate availability, predator avoidance, reduced Allee effects) outweigh the cost of competition (Bowler & Benton, 2005) may decrease dispersal at high population densities (negative density-dependence). During range expansion, spatial selection increases dispersal even when population density is low, so density-dependent dispersal that is less strongly positive, or even negative, may evolve at the range edge (Fig. 1B, dashed line) (De Bona et al., 2019; Fronhofer, Nitsche, et al., 2017; Travis et al., 2009).
Mating status may also influence dispersal decisions for sexually reproducing species that can disperse before and after mating (Clobert et al., 2009; Li & Kokko, 2019; Schumacher et al., 1997). Mated individuals may show positive density-dependent dispersal to reduce competition and reproduce in a low density environment where offspring might have a better chance of survival (Fig. 1B, right), while unmated individuals may show negative density-dependent dispersal to increase the chances of finding a mate (Fig. 1B, left) (Clobert et al., 2009).
We can infer the relative dominance of evolutionary processes during a natural range expansion by evaluating the patterns of key reproductive life-history and dispersal traits across the range. We use the naturally replicated range expansion of an introduced biological control agent (hereafter, biocontrol agent) and examine patterns in life-history and dispersal traits to evaluate drivers of evolutionary change in range expansions in natural populations. This contributes to a growing literature testing range expansion theory on natural populations (Phillips et al., 2006, 2010a; Wolz et al., 2020) and is the first test we know of in a modern biocontrol agent (Szűcs et al., 2019). Understanding the evolutionary dynamics of biocontrol agents is of particular interest for predicting future spread and improving efficacy and safety across the range of a target pest species (Stahlke et al., 2021; Szűcs et al., 2019; Van Klinken & Edwards, 2002; Wright & Bennett, 2018).