doi: 10.1111/j.1420-9101.2011.02255.x Island hopping introduces Polynesian field crickets to novel environments, genetic bottlenecks and rapid evolution R. M. TINGHITELLA*1, M. ZUK*, M. BEVERIDGE &L.W.SIMMONS *Department of Biology, University of California-Riverside, Riverside, CA, USA Centre for Evolutionary Biology, School of Animal Biology, University of Western Australia, Crawley, WA, Australia Keywords: Abstract bottleneck; Teleogryllus oceanicus, a cricket native to Australia, was introduced to Hawaii colonization; where it encounters a novel natural enemy responsible for their recent rapid human migration; evolutionary loss of singing ability. To explore how genetic diversity varies microsatellite; across their broad range, their mode of introduction to Hawaii and nonadap- rapid evolution; tive influences on the sexual signalling system, we assessed variation at seven sexual signal; microsatellite loci in 19 Australian and island populations. Genetic variability Teleogryllus oceanicus. was highest in Australia, intermediate in Oceania and lowest in Hawaii, and differentiation among local populations was a clear function of geographical distance. Hawaiian populations are most closely related to those from the Society Islands and Cook Islands, and a neighbour-joining tree based on DA is consistent with movement by Polynesian settlers. We found evidence of bottlenecks in six island populations (including three Hawaiian populations), supporting previous findings in which bottlenecks were implicated in the crickets’ loss of singing ability. have a broad distribution (Clegg et al., 2002). More Introduction recently, researchers have recognized that many intro- ‘Historical’ or nonadaptive events play an important role duced populations do not exhibit this characteristic in determining the degree of genetic variation present reduction in genetic diversity, perhaps owing to multiple in populations at colonization. Island populations are independent introductions, which merge among-popu- typically founded by very few individuals, resulting in a lation genetic diversity in one location (Calsbeek & ‘founder effect’ (Mayr, 1942), with subsequent genetic Smith, 2003; Wares et al., 2005; Roman & Darling, 2007). reorganization by recombination and drift. As rare alleles In opposition to these forces, we expect ongoing gene are lost and allele frequencies change, recently colonized flow to homogenize populations genetically (Slatkin, populations may experience a reduction in genetic 1987; although recent emphasis has been placed on the diversity relative to their sources as well as rapid ‘multifarious’ effects of gene flow, e.g. Ghalambor et al., differentiation from source populations (Chakraborty & 2007). Nei, 1977; Dlugosch & Parker, 2008). Selection in the Colonization is associated not only with genetic drift novel environment can then act on the genetic variation and bottlenecks, but also with exposure of organisms to in the new population. Under extreme conditions, novel selection pressures, and new populations often colonization processes are thought to be capable of show rapid evolution in novel environments (Reznick initiating reproductive isolation (founder-effect specia- & Ghalambor, 2001). Sexually selected traits may be tion; Mayr, 1942; Coyne & Orr, 2004). These effects are particularly amenable to rapid divergence following particularly well observed after multiple, sequential introduction to new environments (Shaw & Lugo, introductions, as occurs when founding populations 2001; Zuk & Tinghitella, 2008), although rapid evolution of sexually selected characters has been very rarely Correspondence: Robin M. Tinghitella, Department of Biology, observed empirically (Svensson & Gosden, 2007). Such University of California-Riverside, Riverside, CA 92521, USA. Tel.: 517 488 8272; fax: 269 671 2104; e-mail: [email protected] traits, usually male signals and female preferences for 1Present address: Michigan State University, Kellogg Biological Station, them, should be equally as likely as others to experience 3700 East Gull Lake Drive, Hickory Corners, MI 49060, USA. genetic drift and, additionally, are subject to selection ª 2011 THE AUTHORS. J. EVOL. BIOL. 24 (2011) 1199–1211 JOURNAL OF EVOLUTIONARY BIOLOGY ª 2011 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 1199 1200 R. M. TINGHITELLA ET AL. pressures such as the impacts of the environment on moved through most of the Pacific via flight or floating signal transmission, competing signallers and unintended on flotsam, but their limited flight capabilities, short receivers who are attracted to sexual signals (Zuk & generation times and the vast inter-island distances make Kolluru, 1998; Boake, 2002; Zuk & Tinghitella, 2008). it unlikely that they travelled to Hawaii without human Work in Dark-eyed Juncos and field crickets suggests that intervention (Zuk et al., 1998). Intriguingly, T. oceanicus colonizing novel environments does indeed impact the may have been moved through the Pacific intentionally evolution of male sexual signals (Yeh, 2004; Yeh & Price, with the Polynesian settlers (see Discussion). Alterna- 2004; Zuk & Tinghitella, 2008; Tinghitella & Zuk, 2009; tively, they may have travelled on ships in the 19th Tinghitella et al., 2009) and female mating requirements century. (Kaneshiro, 1989; Shaw and Lugo, 2001; Tinghitella & The crickets’ sexual signal is divergent across their Zuk, 2009). Recent rapid evolution in the sexual signal of broad geographic range (Rotenberry et al., 1996; Zuk field crickets in Hawaii (Zuk et al., 2006) affords us an et al., 2001) and selection pressures impacting sexual opportunity to investigate the contributions that popu- signalling vary geographically. On the three Hawaiian lation history makes to rapid evolution following intro- Islands where it occurs (Oahu, Kauai and the Big Island of duction to a novel environment. Hawaii), the cricket encounters a novel natural enemy, a The biota of the central Pacific is predominantly derived parasitoid fly attracted to the male crickets’ song, found from the Western Pacific Rim or continental regions like nowhere else in their range (Cade, 1975; Zuk et al., 1993; Australia and SE Asia (Miller, 1996). Organisms colonize Lehmann, 2003). In Hawaii, males have altered song the Pacific region in one of the two ways: (i) by jumping structure, diel distribution of calling and response to risk, from island to island in a stepping-stone fashion [as relative to those in unparasitized portions of their range, demonstrated by blackflies (Craig et al., 2001; Craig, all of which are consistent with adaptation to avoid the fly 2003), lizards (Austin, 1999) and weevils (Claridge, (Zuk et al., 1993, 1998, 2001; Lewkiewicz & Zuk, 2004). 2006)] or (ii) by repeated independent colonization from These differences are present in laboratory colonies as a mainland source (Gillespie et al., 2008). Far east in the well, suggesting the parasitoid-induced adaptive evolu- Pacific Ocean, the Hawaiian Islands (formed de novo by tionary changes in signalling and behaviour. Most volcanic activity) are no exception, accumulating bio- recently, a mutation in wing morphology on one Hawai- diversity by colonization and subsequent within and ian Island eliminated the crickets’ singing ability alto- between island diversification (Gillespie & Roderick, gether, rendering > 90% of males on the island of Kauai 2002; Whittaker & Ferna´ndez- Palacios, 2007, Garb & obligately mute (Zuk et al., 2006; Tinghitella, 2008). As a Gillespie, 2009). Hawaii is extremely isolated (3200 km result of this mutation, ‘flatwing’, there is some asym- from the nearest continent), and natural colonizations are metric reproductive isolation among populations; females rare, being restricted to exceptional dispersers (Gressitt, from six populations across the crickets’ range do not 1956). Human-aided introductions, however, occur fre- discriminate among males from different populations quently, and human movement patterns may thus drive where song is still produced (accepting on average 83% biological evolution on such islands (Hendry et al., 2000; of males in no-choice courtship trials), but accept only Palumbi, 2001; Hurles et al., 2003; Stockwell et al., 2003; 9–50% of silent ‘flatwing’ males (depending on the Streelman et al., 2004). For instance, Polynesian colonists females’ source population; Tinghitella & Zuk, 2009). If reaching islands in the Pacific purposefully brought with the crickets were taken to Hawaii with humans, this leads them plants and animals for food and agriculture (Keast & to the possibility that anthropogenic disturbance intro- Miller, 1996) and also likely transported others they were duced the crickets to novel environments, which selected not aware of moving. Human-assisted introduction of for dramatic changes in sexual signalling, and consequent these animals impacted the island ecosystems they reproductive isolation. entered in serious and often negative ways (Steadman, Here, we quantify the neutral genetic variation in 1995; Steadman et al., 2002; Hurles et al., 2003). Intro- microsatellites within and among T. oceanicus populations duced organisms, likewise, were affected as they with three aims: (i) to evaluate genetic diversity across responded to novel environmental factors and interacted their range in the Pacific, (ii) to elucidate the crickets’ with previously unencountered organisms. pattern of movement through the Pacific and (iii) to Here, we investigate the genetic differentiation of identify the genetic fingerprint of neutral processes that