Reduced genetic variation and the success of an invasive species

Abstract

Despite the severe ecological and economic damage caused by introduced species, factors that allow invaders to become successful often remain elusive. Of invasive taxa, ants are among the most widespread and harmful. Highly invasive ants are often unicolonial, forming supercolonies in which workers and queens mix freely among physically separate nests. By reducing costs associated with territoriality, unicolonial species can attain high worker densities, allowing them to achieve interspecific dominance. Here we examine the behavior and population genetics of the invasive Argentine ant (Linepithema humile) in its native and introduced ranges, and we provide a mechanism to explain its success as an invader. Using microsatellite markers, we show that a population bottleneck has reduced the genetic diversity of introduced populations. This loss is associated with reduced intraspecific aggression among spatially separate nests, and leads to the formation of interspecifically dominant supercolonies. In contrast, native populations are more genetically variable and exhibit pronounced intraspecific aggression. Although reductions in genetic diversity are generally considered detrimental, these findings provide an example of how a genetic bottleneck can lead to widespread ecological success. In addition, these results provide insights into the origin and evolution of unicoloniality, which is often considered a challenge to kin selection theory.

Figure 1

Sites used in this study. Introduced populations of Argentine ants were sampled in Chile, Bermuda, and the United States. Sampling sites in the United States included New Orleans, Louisiana and the following sites in California: Ukiah (UK), Sausalito (SA), Palo Alto (PA), San Jose (SJ), Salinas (SL), King City (KC), Morro Bay (MB), Santa Maria (SM), Santa Barbara (SB), Los Angeles (LA), Temecula (TE), Encinitas (EN), La Jolla (LJ) and Sweetwater Reservoir (SW). Sites in San Diego County, California not shown: Solana Beach, Lake Hodges and Mission Trails Regional Park. Native populations in Argentina include: Itá-Ibaté (IT), Isla de las Cerritas (IC), Porto Ocampo (OC), Alvear (AL), Parque Nacional PreDelta (PD), Colón (CO), Rosario (RO), Ibicuy (IB), Reserva Nacional Ecológica Otamendi (OT), Buenos Aires (BA), and Reserva Ecológica Costanera Sur (CS). (Bars in the expanded maps represent 100 km.)

Figure 2

Relationship between degree of intraspecific aggression and distance between nest pairs at each of 15 sites within native (A) and introduced (B) ranges of the Argentine ant. Native populations typically exhibited pronounced intraspecific aggression over short distances. In contrast, intraspecific aggression was rare in introduced populations. Aggression between nests was measured by using a behavioral assay ranging from 1 (no aggression) to 4 (high aggression).

Figure 3

Relationships among intraspecific aggression, genetic similarity, and distance at large spatial scales (60–800 km) in native (Argentina, ●) and introduced (California, ○) populations. Aggression between nests was measured by using a behavioral assay ranging from 1 (no aggression) to 4 (high aggression). (A) Relationship of intraspecific aggression and distance between nests. Aggression scores did not overlap between native and introduced populations. All nest pairs in Argentina displayed high levels of aggression, whereas nest pairs in California did not. (B) Genetic similarity between nests versus distance. Nest pairs in California shared at least 75% of alleles. In contrast, 17–63% of alleles were shared between nest pairs in Argentina. (C) Relationship between aggression and genetic similarity of nests. In California, aggression was absent and nests were genetically similar, whereas in the native range the opposite pattern held.

Figure 4

Relationship of aggression between nests and their genetic similarity. Aggression between nests was measured by using a behavioral assay ranging from 1 (no aggression) to 4 (high aggression). For this analysis, extensive sampling was necessary to locate nest pairs that exhibited intraspecific aggression within California. Average aggression decreased with increasing genetic similarity in both Argentina (A; 29 nest pairs, y = 5.48 − 0.046x) and California (B; 83 nest pairs, y = 5.37 − 0.042x). The slopes and intercepts of these regressions did not differ (t tests, P > 0.5). Additionally, adding the nest pairs from the long distance comparisons (Fig. 3) increases significance.