Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird

Abstract

Behaviors can facilitate colonization of a novel environment, but the mechanisms underlying this process are poorly understood. On one hand, behavioral flexibility allows for an immediate response of colonizers to novel environments, which is critical to population establishment and persistence. On the other hand, integrated sets of behaviors that display limited flexibility can enhance invasion success by coupling behaviors with dispersal strategies that are especially important during natural range expansions. Direct observations of colonization events are required to determine the mechanisms underlying changes in behavior associated with colonization, but such observations are rare. Here, we studied changes in aggression on a large temporal and spatial scale across populations of two sister taxa of bluebirds (Sialia) to show that coupling of aggression and dispersal strongly facilitated the range expansion of western bluebirds across the northwestern United States over the last 30 years. We show that biased dispersal of highly aggressive males to the invasion front allowed western bluebirds to displace less aggressive mountain bluebirds. However, once mountain bluebirds were excluded, aggression of western bluebirds decreased rapidly across consecutive generations in concordance with local selection on highly heritable aggressive behavior. Further, the observed adaptive microevolution of aggression was accelerated by the link between dispersal propensity and aggression. Importantly, our results show that behavioral changes among populations were not caused by behavioral flexibility and instead strongly implicate adaptive integration of dispersal and aggression in facilitating the ongoing and rapid reciprocal range change of these species in North America.

Fig. 1.

Changes in the breeding range of western bluebirds in Montana from 1975 to 2005. Data on aggressive behavior were collected from eight nest box populations near the towns of St. Regis (STR), Perma (PER), Moiese Valley (MV), Missoula (BMT and UMC), Hamilton (HMT), Ovando (OVD), and Stanford (STF). Pie charts indicate the relative proportion of western (white) and mountain (black) bluebirds breeding in each of the study populations during 2001–2005 (summed over 5 years). Before 1975, all mapped populations were comprised of 100% mountain bluebirds. (Inset) Rapid displacement of mountain bluebirds by western bluebirds in BMT (Upper) (western: n = 224; mountain: n = 78) and UMC (Lower) populations (western: n = 38; mountain: n = 134). Dashed lines represent mountain bluebirds, and solid lines represent western bluebirds. Gray lines indicate estimated trend.

Fig. 2.

Variation in aggression across species, populations, generations, and dispersal classes. (A) Western bluebirds were more aggressive than mountain bluebirds. (B) Aggression differed significantly among western bluebird populations and was related to the number of years since colonization of a population (numbers above bars) See Fig. 1 for location abbreviations and supporting information (SI) Table 1 for sample sizes. (C) Aggression significantly decreased across cohorts in the BMT population. (D) Males that dispersed away from their natal population to breed (Left) were more aggressive than males that remained in their natal population (Right). Shown are means ± SE. Numbers on bars indicate the number of males sampled.

Fig. 3.

Significant negative selection on aggression in the BMT population, where mountain bluebirds were excluded in 2001. Reproductive success is calculated as the residuals of a regression of a male's annual reproductive success and age. The sizes of the circles indicate the number of overlapping data points with the smallest size indicating a single point and the largest indicating three overlapping points.