Island Hopping Introduces Polynesian Field Crickets to Novel Environments

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 & Fernańdez- 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 Polynesian field crickets, Teleogryllus oceanicus (Orthop- might influence sexual signal evolution in this group tera: Gryllidae), and the manner in which they moved (bottlenecks and gene flow). through the Pacific to better understand the nonadaptive forces responsible for their introduction to Hawaii and Methods the subsequent rapid evolution of their sexual signalling system. The cricket is native to northern regions of the Genetic analysis Australian continent, found on numerous Pacific Islands, and was introduced to Hawaii sometime prior to 1877 Samples for DNA analysis were collected from nineteen (Kevan, 1990; Otte, 1994). Teleogryllus oceanicus may have locations in Australia and on Pacific islands (Fig. 1,

ª 2011 THE AUTHORS. J. EVOL. BIOL. 24 (2011) 1199–1211 JOURNAL OF EVOLUTIONARY BIOLOGY ª 2011 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY Polynesian crickets hitchhike to rapid evolution 1201

Fig. 1 Geographic distribution of nineteen Teleogryllus oceanicus populations sampled in Northern and Eastern Australia, across numerous Paciﬁc Islands, and in their introduced range of Hawaii. In three cases (Hawaii, Fiji and the Cook Islands), multiple island populations were sampled from a given island chain.

Table 1) between 2004 and 2007, including eight loca- for 1 min, and 72 C for 1 min and finally 72 C for tions in the putatively ancestral range (A = Australia), 45 min. We analysed the products on an ABI 3100 eight island populations from the portion of the range Genetic Analyzer and sized alleles using a LIZ internal where the cricket and fly do not overlap (O = Oceania) size standard and GENEMAPPER V3.7(2) software (opti- and three Hawaiian populations from the parasitized mizing sizing by eye). portion of the crickets’ range (H = Hawaii). Seven of We screened 394 samples from nineteen mainland these populations were part of an earlier study of genetic Australian and Pacific Island populations with sample distance and sensoribehavioural regression in T. oceanicus sizes ranging from 5 to 25 individuals per population (Fullard et al., 2010). Geographic distances between (Table 1). We assessed whether populations were in sampled localities ranged from 83 km (between Cook- Hardy–Weinberg equilibrium at each locus using GENE- town and the Daintree region in eastern Australia) to POP 3.4 (Raymond & Rousset, 1995). Six loci were in 11 582 km (between Broome, Australia and Hiva Oa, equilibrium (one population per locus was out of Marquesas) (Tables 2 and 3). We removed one leg from equilibrium after Bonferroni correction), but locus each cricket, dissected out the femur muscle and stored Totri88a was out of equilibrium in > 70% of the the samples in ethanol at )80 C until the time of DNA populations studied. This is consistent with Beveridge & extraction. DNA was extracted using a standard salt Simmons (2005) observation that this locus shows extraction protocol, and neutral genetic variation was null alleles and appears to be X-linked. We therefore assayed at seven highly polymorphic microsatellite omitted the seventh locus, Totri88a, and concentrated loci developed specifically for T. oceanicus (Beveridge & our analyses on the remaining six loci that amplify Simmons, 2005). cleanly and have the fewest null alleles based on Hardy– Each 15-lL PCR contained 1 · PCR buffer (10 mM Tris– Weinberg equilibrium. This left Totri 9a, Totri 54, Totri HCl pH 8.3, 50 mM KCl), 1.5 mM or 3.5 mM MgCl2 (see 55a, Totri 57, Totri 59 and Totri 78. Linkage disequili- Beveridge & Simmons, 2005 for details; Invitrogen, brium was assessed for each locus pair within each Carlsbad, CA, USA), 200 lM of each dNTP (Invitrogen), population and across all populations using the genotypic 250 nM of the forward primer (labelled and unlabelled in disequilibrium option in GENEPOP version 3.4. Totri a ratio of 1 : 5), 250 nM of the reverse primer (Integrated 9a and Totri 57 were found to be in disequilibrium, DNA Technologies), 1 unit of Platinum Taq DNA poly- indicating the two may not segregate independently, but merase (Invitrogen) and 10ng of DNA. PCR amplifica- were only in disequilibrium in three of the 19 population was performed with the following cycling conditions: tions, namely Vanuatu, Samoa and Kauai. We retained 94 C for 1 min, then 30 cycles at 94 C for 1 min, 55 C both loci in this study.

ª 2011 THE AUTHORS. J. EVOL. BIOL. 24 (2011) 1199–1211 JOURNAL OF EVOLUTIONARY BIOLOGY ª 2011 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 1202 R. M. TINGHITELLA ET AL.

Table 1 Allelic diversity, allelic richness (AR), heterozygosity and bottlenecks in the nineteen Teleogryllus oceanicus populations. Samples are ordered roughly from west to east in their geographic distribution. Regions are Australia (A: mainland populations), Oceania (O: nonparasitized island populations) and Hawaii (H: parasitized island populations in the crickets’ introduced range of Hawaii). Primers are 1 = Totri 9a, 2 = Totri 54, 3 = Totri 55a, 4 = Totri 57, 5 = Totri 59 and 6 = Totri 78 (after Beveridge & Simmons, 2005). In the Allelic diversity ⁄ Allelic richness column, NA can be found above and AR below. AR is based on a minimum sample size of four diploid individuals and was calculated using FSTAT. BOTTLENECK estimates heterozygote excess when compared with expected equilibrium heterozygosity. Signiﬁcance of the BOTTLENECK results was estimated by Wilcoxin signed-rank tests (P < 0.05).

Allelic diversity (NA) & AR by locus Mean BOTTLENECK

Sample n 123 456NA AR HE (IAM ⁄ SMM ⁄ TPM)

Australia (A) 159 71 71 109 91 71 84 497 Carnarvon 22 8 6 10 13 8 11 56 5.065 0.836375 + ⁄ ) ⁄ ) 4.815 3.674 5.908 6.170 4.637 5.188 Broome 20 10 11 19 15 12 11 78 5.539 0.849887 ) ⁄ ) ⁄ ) 5.422 5.414 6.979 6.063 3.662 5.692 Darwin 10 6 5 7917354.966 0.729798 ) ⁄ ) ⁄ ) 6.000 4.378 6.133 6.308 1 5.978 Kunnunura 22 9 9 13 13 9 12 65 5.195 0.803631 ) ⁄ ) ⁄ ) 5.180 4.872 6.171 6.360 2.928 5.659 Cooktown 22 9 9 12 7 9 12 58 4.745 0.786283 ) ⁄ ) ⁄ ) 5.160 4.810 5.553 3.937 3.254 5.754 Daintree 19 10 11 13 10 8 9 61 5.176 0.846231 ) ⁄ ) ⁄ ) 5.455 5.280 6.187 4.713 3.962 5.461 Cairns 21 11 10 19 11 12 11 74 5.273 0.837901 ) ⁄ ) ⁄ ) 5.239 5.115 6.923 3.925 4.869 5.568 Mission Beach 23 8 10 16 13 12 11 70 5.298 0.838534 ) ⁄ ) ⁄ ) 5.260 4.560 6.840 4.296 5.171 5.662 Oceania (O) 162 30 45 77 40 51 43 286 Efate, Vanuatu 24 5 8 12 749454.003 0.698906 ) ⁄ ) ⁄ ) 2.918 3.916 5.751 3.871 2.082 5.481 Viti Levu, Fiji 20 4 5 13 6 10 7 45 4.269 0.756145 + ⁄ ) ⁄ ) 3.251 3.499 6.362 4.194 4.411 3.898 Vanua Levu, Fiji 20 5 8 10 6 11 7 47 4.292 0.760558 ) ⁄ ) ⁄ ) 3.189 4.065 5.383 4.148 4.685 4.281 Upolu, Samoa 25 4 7 11 565383.574 0.644544 ) ⁄ ) ⁄ ) 2.275 4.157 5.420 3.736 3.194 2.660 Atiu, Cook Islands 5 3 4 4343213.182 0.608333 ) ⁄ ) ⁄ ) 2.956 3.400 3.578 2.956 3.400 2.800 Rarotonga, Cook Islands 18 5 5 10 462323.814 0.685892 + ⁄ ) ⁄ ) 3.819 3.236 6.333 3.361 4.147 1.988 Moorea, Society Islands 25 3 7 8365323.414 0.639832 + ⁄ ) ⁄ ) 2.262 4.062 5.045 2.453 3.699 2.964 Atuona, Marquesas 25 1 1 9645262.558 0.392766 ) ⁄ ) ⁄ ) 1 1 5.015 3.745 2.108 2.479 Hawaii (H) 73 7 16 20 14 13 9 80 Oahu 24 3 6 7555313.421 0.623423 + ⁄ ) ⁄ ) 2.453 4.452 4.193 3.886 2.988 2.555 Hawaii 24 2 5 4442212.615 0.515700 + ⁄ ) ⁄ ) 1.979 3.647 3.047 2.958 2.444 1.616 Kauai 25 2 6 9542282.984 0.522880 + ⁄ ) ⁄ ) 1.822 4.238 4.935 3.292 2.205 1.414

Allelic diversity (NA; for each population and locus and 2.9.3.2 (for AR; Goudet, 1995; Tables 1 and 2). Genetic pooled across the six loci), allelic richness (AR) and mean distances were then used in conjunction with population AR per population, expected heterozygosity (calculated pairwise geographic distances calculated using a surface using Levene’s corretion for small sample size) and a distance calculator (http://www.chemical-ecology.net/ matrix of pairwise genetic distances (FST estimated by java/lat-long.htm) to test for isolation by distance using Weir & Cockerham, 1984) were produced using GENEPOP the ISOLDE option in GENEPOP version 3.4. A Mantel test version 3.4 (Raymond & Rousset, 1995) and FSTAT version with 1000 permutations assessed how well geographic

ª 2011 THE AUTHORS. J. EVOL. BIOL. 24 (2011) 1199–1211 JOURNAL OF EVOLUTIONARY BIOLOGY ª 2011 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY ORA FEOUINR BIOLOGY EVOLUTIONARY OF JOURNAL ª Table 2 Population pairwise differentiation (FST ) among 19 populations of Teleogryllus oceanicus. Pairwise FST values were estimated as in Weir & Cockerham (1984) using GENEPOP version 01TEAUTHORS. THE 2011 3.4 on the web.

Mission Viti Vanua Carnarvon Broome Kununurrra Darwin Cooktown Daintree Cairns Beach Vanuatu Levu Levu Samoa Atiu Rarotonga Moorea Marquesas Oahu Hilo

Broome 0.0326 Kununurrra 0.0284 )0.006 Darwin 0.096 0.0264 0.0089 .EO.BIOL. EVOL. J. Cooktown 0.0616 0.0292 0.0217 0.0498 Daintree 0.0477 0.0249 0.0234 0.0699 0.0064 Cairns 0.0601 0.0428 0.0414 0.0834 0.0118 0.0052 Mission Beach 0.0497 0.0373 0.0336 0.0698 0.008 0.0093 )0.0074 Vanuatu 0.0902 0.1448 0.1453 0.2184 0.1089 0.1036 0.0902 0.1168

24 Viti Levu 0.0756 0.0841 0.0771 0.1545 0.0672 0.0612 0.079 0.088 0.0729 ª Vanau Levu 0.0715 0.0679 0.0632 0.1376 0.0378 0.0365 0.058 0.0626 0.0888 0.0042 21)1199–1211 (2011) 01ERPA OIT O VLTOAYBIOLOGY EVOLUTIONARY FOR SOCIETY EUROPEAN 2011 Samoa 0.1677 0.1865 0.1886 0.2637 0.159 0.1384 0.1573 0.1602 0.1104 0.1011 0.094 Atiu 0.1655 0.1238 0.1341 0.1559 0.1476 0.1302 0.1519 0.1404 0.2433 0.1632 0.1385 0.2017 Rarotonga 0.1326 0.1398 0.1455 0.1833 0.143 0.1129 0.1419 0.132 0.1832 0.1213 0.1288 0.1176 0.0491 Moorea 0.1259 0.1258 0.1228 0.1893 0.138 0.1169 0.1414 0.1365 0.1813 0.1218 0.1075 0.1089 0.0956 0.0923 Marquesas 0.3086 0.3122 0.3224 0.4298 0.2721 0.2614 0.2698 0.2886 0.1874 0.2296 0.2137 0.1554 0.3524 0.2892 0.2241 Oahu 0.133 0.1306 0.1297 0.2022 0.1301 0.1368 0.1679 0.1529 0.2625 0.1682 0.163 0.2256 0.1599 0.1267 0.1472 0.3842 Hilo 0.1842 0.1874 0.1842 0.2609 0.1766 0.1847 0.2329 0.2203 0.3005 0.1804 0.1738 0.2257 0.1848 0.1543 0.1363 0.3693 0.0442 Kauai 0.1944 0.1913 0.1851 0.2625 0.17 0.175 0.2218 0.2093 0.3113 0.1882 0.1844 0.2401 0.2205 0.1498 0.1676 0.4174 0.0369 0.027

Table 3 Population pairwise geographic distances (km) were calculated using a surface distance calculator available at (http://www.wcrl.ars.usda.gov/cec/java/lat-long.htm).

Mission Viti Vanua

Carnarvon Broome Kununurrra Darwin Cooktown Daintree Cairns Beach Vanuatu Levu Levu Samoa Atiu Rarotonga Moorea Marquesas Oahu Hilo evolution rapid to hitchhike crickets Polynesian

Broome 775.78 Kununurra 1866.69 1766.01 Darwin 2269.37 2087.21 438.46 Cooktown 3442.71 3519.6 1772.58 1591.53 Daintree 3416.35 3512.32 1775.17 1614.11 83.51 Cairns 3431.75 3547.87 1822.07 1678.21 169.17 90.44 Mission Beach 3428.08 3570.93 1863.71 1744.44 285.74 240.06 116.56 Vanuatu 5674.12 5905.39 4213.54 4056.45 2465.31 2448.24 2393.79 2350.5 Viti Levu 6604.86 6866.4 5185.3 5028.07 3437.48 3421.05 3366.47 3321.72 972.84 Vanua Levu 6614.59 7070.07 5381.28 5002.84 3414.34 3613. 06 3348.45 3518.61 1168.19 213.81 Samoa 7826.22 8080.71 6381.8 6200.48 4618.64 4608. 82 3922.07 4522.24 2175.54 1221.53 1012.76 Atiu 8906.62 9288.71 7692.26 7574.64 5985.16 5960.54 5898.16 5840.09 3532.67 2578.16 2416.71 1601.53 Rarotonga 8697.09 9086.52 7501.53 7391.86 5804.5 5778.01 5714.14 5653.8 3360.41 2416.73 2264.53 1510.1 217.24 Moorea 11443.74 10181.01 8582.96 8458.54 6867.61 6844.95 6784.06 6728.01 4407.61 3443.64 3270.7 2371.39 893.22 1095.21 Marquesas 11239.29 11582.13 9920.26 9749.07 8164.8 8152. 39 8100.16 8056.75 5706.83 4735.02 4539.68 3548.73 2344.59 2559.13 1496.37 Oahu 10824.63 10701.54 8993.85 8624.84 7422.03 7461.82 7464.71 7495.62 5688.18 5077.88 4889.7 4188.33 4596.35 4734.24 4441.75 3924.24

Hilo 11023.32 10933.07 9208.17 8849.56 7600.09 7636.14 7634.44 7659.56 5766.75 5103.94 4908.54 4148.91 4429 4578.72 4213.87 3618.07 302.04 1203 Kauai 10750.07 10568.76 8870.57 8540.35 7318.28 7359.95 7365.18 7399.02 5638.37 5056.95 4873.01 4204.27 4678.33 4809.7 4555.91 4080.94 181.84 526.72 1204 R. M. TINGHITELLA ET AL.

distance estimated genetic distance. Geographic trends NA was highest in the Australian region (which includes in the measures of genetic diversity were assessed by eight Australian populations distributed from the mid- regressing the expected heterozygosities and allelic rich- coastal regions of Western Australia to the NE coast), nesses against longitude. Also, for the three measures of intermediate in Oceania and lowest in the Hawaiian genetic diversity (HO, HE and AR), and population differ- Islands (Table 1). The lowest levels of allelic diversity were entiation (FST), a group comparison according to region found on Atiu in the Cook Islands and the Big Island of (Australia, Oceania, Hawaii) was performed with permu- Hawaii; each had only 21 alleles summed across the six tation tests in FSTAT. We asked whether the 19 populations loci. Low allelic diversity in Atiu is likely due, at least had recently experienced severe reductions in effective partially, to the small number of samples collected there. population size using BOTTLENECK version 1.2.02 (Piry The NW Australian population of Broome was the most et al., 1999). BOTTLENECK estimates observed hetero- diverse, with 78, followed by Cairns with 74 alleles. The zygosity excess relative to expected equilibrium hetero- highest allele richness, with an average of 5.539 alleles, zygosity. We performed the tests using all three options per locus was found in Broome and the lowest in the available in BOTTLENECK, the infinite alleles model (IAM; Marquesas, with an average of 2.558 alleles (Table 1). We Kimura & Crow, 1964), stepwise mutation model found evidence of only one allele at two loci in the (SMM; Ohta & Kimura, 1973) and the two-phase model Marquesas population (at Totri 9a, Totri 54) and at one (TPM; probability of SMM 70%, variance 30%; Di Rienzo locus in the Darwin, Australia population (Totri 59). et al., 1994), and significance was assessed with Wilcoxon Levels of gene diversity (HE) within populations ranged signed-rank tests (P < 0.05; Table 1) (Cornuet & Luikart, from a high of 0.849 in the Western Australian population 1996). of Broome to a low of 0.393 in the island population of DA distances (Nei et al., 1983) were calculated based on Hiva Oa, Marquesas (Table 1). When testing for geo- microsatellite data for all populations with 1000 ran- graphical trends in genetic diversity, the highest genetic domized permutations to assess statistical support using diversities were found in the western portion of the Microsatellite Analyser (MSA; Deiringer & Schlotterer, crickets’ range, and diversity (measured as both HE and 2002). Takezaki & Nei (2008) demonstrated that the AR) decreased from west to east (R2 = 0.7278, 2 probability of obtaining the correct branching pattern in F1,16 = 42.78, P < 0.001 and R = 0.8959, F1,16 = 137.77, a tree built on microsatellite data is highest when using P < 0.001 respectively). Figure 2 demonstrates the char- the standard genetic distance, DA, which is thought to acteristic reduction in allelic diversity noted across the increase roughly linearly with time since separation crickets’ distribution using the distribution of alleles at just (assuming a low mutation rate, Slatkin, 1995). To assess one representative locus, Totri 9a. Indeed, island popula- sources for populations introduced to Hawaii and estab- tions appear to have fewer alleles at each locus, and the lish the likely route of Pacific colonization, relatedness characteristic bottleneck ‘shape’ is apparent. trees were constructed using DA in PHYLIP Version 3.65 On average, the Australian region had significantly (Felsenstein, 2005). The data set was first converted to higher AR and gene diversity than the Oceania and Hawaii PHYLIP’s preferred format, a gene frequency format, using regions (Table 4) following permutation tests in FSTAT. the program CONVERT version 1.31 (Glaubitz, 2004). Pairwise FST and observed heterozygosity (HO), however, Bootstrap values (500 replications) were calculated using did not differ significantly among the three regions SEQBOOT, and unrooted consensus neighbour-joining (P = 0.218 and P = 0.148 respectively, Table 4). That trees were obtained using the following sequence: Australian populations are not more genetically distinct SEQBOOT, GENDIST, NEIGHBOR and DRAWTREE. Trees from one another than Hawaiian populations, for instance, were visualized with the software TREEEDIT version 1.0 is consistent with the low pairwise FST values found among (Rambaut & Charleston, 2000). Finally, global migration Australian populations (despite the vast inter-population was estimated using the private alleles method (Barton & distances) and within island chains (see below). Slatkin, 1986) in GENEPOP version 3.4 on the web. Pairwise genetic differentiation (FST) estimated as in Weir & Cockerham (1984) ranged from a low of 0.0042 Results (between two Fijian islands of Viti Levu and Vanua Levu) to a high of 0.4374 between the Hawaiian island of Kauai Six highly polymorphic loci with 14–31 alleles per locus and the Marquesas (an island nation 4080 km SE of were sampled in 19 populations across the broad Pacific Hawaii; Tables 2 and 3). In three locations, we were able range of T. oceanicus. Alleles per locus were as follows: to sample multiple islands within an island chain (Atiu Totri 9a had 14, Totri 54 had 21, Totri 55 had 31, Totri 57 and Rarotonga in the Cook Islands, Viti Levu and Vanua had 26, Totri 59 had 25, and Totri 78 had 14. Allelic Levu in Fiji and Oahu, Hawaii and Kauai in Hawaii). In diversity (NA) and AR decreased roughly from west to east, all three cases, pairwise population differentiation values both when observed at individual loci and when summed within the island chains were among the lowest we (or averaged for AR) across the six loci (Table 1), consis- observed (ranging from 0.0042 to 0.0491). Pairwise tent with a spread of the cricket from their native Australia population differentiation also remains low among to the islands of the Pacific via a series of serial bottlenecks. Australian populations, ranging from 0.0052 to 0.0616,

ª 2011 THE AUTHORS. J. EVOL. BIOL. 24 (2011) 1199–1211 JOURNAL OF EVOLUTIONARY BIOLOGY ª 2011 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY Polynesian crickets hitchhike to rapid evolution 1205

Fig. 2 Allele size distribution of a representative Teleogryllus oceanicus locus (Totri 9a) across the crickets’ broad distribution. All plots use the same scale. There is a characteristic reduction in allelic diversity, as you move from west to east in the crickets’ distribution consistent with their introduction to Paciﬁc islands from their native range in Australia. Notice the characteristic ‘bottleneck effect’ in island populations. Allelic diversity is signiﬁcantly lower in the Oceania region relative to Australia and in the Hawaiian region relative to Oceania.

Table 4 Comparison of allelic richness (AR), observed heterozy- (1), Cooktown (1), Samoa (5) and Viti Levu (1). We did, gosity (HO), gene diversity (HE) and levels of differentiation (FST) however, find evidence of ongoing gene flow across the among populations for the Australian, Oceanic and Hawaiian crickets’ range. Global migration was assessed using regions of Teleogryllus oceanicus distribution. the private alleles method (Barton & Slatkin, 1986), and the number of migrants was estimated to be 2.595 per N (populations) AR** HO HE* FST generation after correction for sample size. Australia 8 5.156 0.689 0.830 0.030 Signs of recent bottlenecks (using the program BOT- Oceania 8 3.638 0.563 0.641 0.146 TLENECK) were noted in only one Australian population Hawaii 3 3.007 0.570 0.557 0.037 (Carnarvon), three of the eight island populations in the Significance levels were *P < 0.01, **P < 0.001 following permuta- Oceania group (Viti Levu, Rarotonga, and Moorea) and tion tests in FSTAT. all three of the Hawaiian Island populations tested (Table 1). Despite the low heterozygosity and AR noted in the Marquesas population (Table 1), no recent bottle- despite the vast geographic distances separating these neck was evident, but this may be an artefact of high populations (up to 3571 km). Marquesas consistently homozygosity in the Marquesas; two loci in this popu- returned some of the largest measures of pairwise lation revealed only one allele each and therefore 0% population differentiation we observed, ranging from a heterozygosity. Having a single allele at each of these loci low of 0.1534 with Samoa (3548 km away) to 0.4374 is consistent with a founder effect. with Kauai, Hawaii (4080 km NW of the Marquesas). Neighbour-joining analysis based on DA revealed sev- We found a strong pattern of isolation by distance (as eral well-supported groupings of populations (Fig. 4). For assessed by Mantel test with 1000 permutations in GENE- the most part, these represent regional clusters – POP V3.4 ISOLDE) in the data set, indicating restricted gene Australia, and two clusters within Oceania (A = Vanuatu, flow among the samples in accordance with geographic Fiji, Samoa, Marquesas, and B = Cook Islands, Society distances (Spearman Rank Correlation, r = 1.0, N (total Islands, Hawaiian Islands). comparisons) = 153, P = 0.000; Fig. 3). The 19 unique, or private, alleles in the data set were distributed among the Discussion following eight populations (number of private alleles per population indicated in parentheses): Cairns (5), Despite their recent spread through the Pacific, Polyne- Broome (2), Daintree (2), Carnarvon (1), Mission Beach sian field cricket populations are highly structured.

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and modify such reduction in diversity. For example, contemporary admixture may be greater than historical levels because human movement through the Pacific removes a barrier to dispersal – the vast open ocean distances between islands. This can make reconstruction of historical population relationships difficult. The pattern of genetic diversity loss in our data agrees with earlier suggestions that T. oceanicus was introduced to the western Pacific islands from their native Australia and then spread progressively further east, arriving most recently in remote locations such as the Hawaiian Islands and the Marquesas (Otte, 1994). Our analyses suggest a loss of allelic diversity (NA), AR and expected heterozygosity (HE) moving east through the crickets’ Fig. 3 Isolation by distance. There is a strong pattern of isolation by distribution (Tables 1 and 4, Fig. 2). This pattern is not distance in the data set indicating restricted gene flow among the universally observed in introduced island populations, samples in accordance with geographic distances. Points circled however. Several recent studies have found increased represent relationships between the Marquesas population and other levels of diversity when multiple introductions were mainland Australian or island populations. These population pairs experienced the highest genetic distances, although they are not made from different locations (Calsbeek & Smith, 2003; always particularly geographically distant from one another relative Wares et al., 2005; Roman & Darling, 2007). We suggest to other pairs studied, highlighting the apparent genetic isolation of that the probability of multiple colonization events is the Marquesas (Table 3). In contrast, the points enclosed in the likely to decrease with distance to source populations shaded box (lower left) represent select population pairs within and hostility of the environment into which introduc- Australia or within an island chain, where gene flow appears to tions are made. Because the movement of T. oceanicus homogenize populations genetically, in some cases despite vast was relatively linear as west to east colonization geographic distances. For instance, Broome and Kununurra are progressed, the likelihood of multiple introductions separated by 1766 km. (a) Marquesas ⁄ Atiu, Cook Islands, (b) from the source (Australia) to any given island is low Marquesas ⁄ Hilo, HI, (c) Marquesas ⁄ Oahu, HI, (d) Marquesas ⁄ Kauai, and not supported. We also found a clear pattern of HI, (e) Marquesas ⁄ Darwin, Australia. Shaded points include Viti isolation by distance, indicating restricted gene flow Levu, Fiji ⁄ Vanua Levu, Fiji (Fst = 0.0042), Broome, Australia ⁄ among the samples in accordance with geographic Kununurra, Australia (Fst = 0.006), Cairns, Australia ⁄ Mission

Beach, Australia (Fst = 0.0074), Mission Beach, Australia ⁄ distance (Fig. 3). This might be expected among island

Cooktown, Australia (Fst = 0.008), Darwin, Australia ⁄ Kununurra, populations as the open ocean serves as a barrier to Australia (Fst = 0.0089) and Daintree, Australia ⁄ Mission Beach, organisms with limited dispersal ability and suggests Australia (Fst = 0.0093). that T. oceanicus populations in the Paciﬁc have reached an equilibrium between migration and drift.

Genetic variability decreased from west to east through Island hopping through the Pacific their distribution and differentiation among local populations was a clear function of geographical distance. Our proposed route of colonization, from west to east, is Genetic relationships based on microsatellite data suggest further supported by relationships among populations the Hawaiian populations are least distant from those in noted in our consensus neighbour-joining tree. Our Moorea (in the Society Islands) and the two populations findings suggest that Hawaiian populations are most from the Cook Islands. Finally, we found evidence of closely related to those from the Society Islands and the genetic bottlenecks in one mainland and six island Cook Islands (Fig. 4). Intriguingly, this is consistent with populations (three outside of Hawaii as well as all three some models of human movement during the Polynesian Hawaiian islands sampled), a nonadaptive process expansion. Polynesian folklore indicates the calls of thought to have consequences for the evolution of sexual crickets are thought to represent the cries of dead signalling systems in general (Kaneshiro, 1989), and for ancestors (in Loher & Orsak, 1985) and crickets figure T. oceanicus in particular (Tinghitella & Zuk, 2009). We prominently in Polynesian spirit traditions (Clerk, 1990). discuss each of these results in turn below. If Polynesian settlers aided the dispersal of the crickets, we would expect the genetic relationships among cricket populations to reflect the patterns of human movement Genetic diversity across the Pacific during the Polynesian expansion (see Fig. 5). Human Although theory suggests that genetic diversity should colonization of eastern Polynesia may have occurred decrease along a colonization route (Hewitt, 1996; from a broad central region encompassing the Societies Austerlitz et al., 1997), both historical and contemporary and the Cooks, but probably not the Marquesas, with at factors can impact genetic structuring of populations least two introductions to Hawaii (from the Societies and

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Fig. 4 Unrooted consensus (500 bootstrap replications) Neighbour-Joining tree based on DA. Three groups corresponding roughly to geographic locations can be seen: (i) Australian populations, (ii) Fiji, Vanuatu, Samoa and Marquesas and (iii) Hawaii + Moorea (Society Islands) and the Cook Islands of Atiu and Rarotonga. The close relationship between Hawaiian populations and the group Moorea + Cook Islands suggests the Hawaiian crickets are derived from one of these two locations. the Marquesas) (Matisoo-Smith et al., 1998). Our find- isolated is consistent with evidence from genetic diversity ings are not consistent with introduction to Hawaii from in populations of the Pacific rat, a commensal of humans the Marquesas (with humans or otherwise). The close moved in canoes with Polynesian settlers (Matisoo-Smith relationships between crickets from Hawaii and the et al., 1998). Such isolation is in contrast to earlier views Societies ⁄ Cooks, and those from Samoa and the in which the Marquesas are considered to be central in Marquesas (Fig. 4), however, are consistent with eastern Polynesian interaction and contact (Kirch, 1985). Matisoo-Smith et al.’s (1998) model of human-aided Much debate still surrounds this issue (Kirch & Kahn, dispersal. Within Hawaii, Oahu has the highest levels of 2007), and evidence from a range of different fields, genetic diversity (Table 1) followed by Kauai and Hawaii, including genetic studies of plants and animals moved suggesting that of these three, Oahu was settled first. with Polynesian settlers, suggests human settlement in The second grouping of island populations in our the Pacific is far more complex than simple models such neighbour-joining relationship tree is consistent with as the ‘Express Train’ or ‘Entangled Bank’ (Hurles et al., patterns of pre-European contact human movement in 2003). Analysing mitochondrial sequences, in addition to the Pacific as well (Fig. 4). Before the Society Islands and microsatellite loci, and sampling more extensively in the Marquesas became the locations from which colonizers Pacific would be especially informative for addressing ventured out, Fiji, Vanuatu, Samoa and the Marquesas questions of multiple introductions to remote Oceania were settled. That the Marquesas appear to be very and Hawaii, for corroborating the relationships among

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Fig. 5 Human migration patterns during the Polynesian expansion, following the ‘Express Train to Polynesia’ hypothesis. Polynesian settlers are thought to have their origins in SE Asia. Near Oceania (Bismarck, Solomon Islands) was settled by non-Austronesian speaking people between 40 and 60 000 years BP (Summerhayes et al., 2010). Remote Oceania (Vanuatu, Fiji, Tonga, Samoa, New Caledonia) was settled by 3100 BP at the earliest, with Samoa and Tonga settled by 2900 BP (Kirch, 2000; Hurles et al., 2003; Bedford et al., 2006). The appearance of Lapita (and assumed arrival of Austronesian expansion into Near Oceania) is about 3350 BP. The two best-known scenarios for Paciﬁc colonization include the ‘Express Train’ characterized by the simple spread of Polynesian ancestors into Near Oceania then Remote Oceania with little genetic exchange (pictured here), and the ‘Entangled Bank’, a reticulate model postulating ongoing interaction among populations (Hurles et al., 2003). Human mitochondrial DNA studies also support a third hypothesis, the ‘Slow Boat’ or ‘Slow Train’ in which more genetic mixture occurred before humans reached Remote Oceania (Hurles et al., 2003). Broken arrows indicate proposed movement in the region between approximately 3500–2700 years BP, and solid arrows indicate movement in the region between 1200 and 500 years BP (the settlement of East Polynesia and Polynesian outliers; following Addison & Matisoo-Smith, 2010).

Pacific populations of T. oceanicus and for dating the did not find evidence of a bottleneck in the Marquesas, crickets’ arrival to Hawaii (either 1500 years ago with despite those islands’ low allelic diversity and heterozy- Polynesian settlers or more recently travelling on ships gosity which suggests extreme isolation and low ongoing post-European settlement). Sampling in New Guinea, gene flow (Table 1). This may be because of finding only the Bismarck Archipelago and the Solomon Islands, for a single allele at each of two loci in the Marquesan instance, would allow us to address the timing of population. Monomorphic loci contribute nothing to dispersal into Remote Oceania. We suspect the cricket heterozygosity, and BOTTLENECK estimates the likelihood may also be native to New Guinea (possibly to Sahul and of a genetic bottleneck as an increase in observed therefore New Guinea and Australia), as it is found on heterozygosity. Finding monomorphic loci might make the tip of Cape York (Otte & Alexander, 1983), but we such an observation highly unlikely. are unaware of references stating absolutely whether The discovery of bottlenecks is relevant to the spread of that is so. the flatwing mutation in Hawaii. Previous work suggests that genetic bottlenecks led to the relaxation of female mating requirements in Hawaiian T. oceanicus popula- Nonadaptive contributions to variation in sexual tions relative to other island and mainland populations. signalling Tinghitella & Zuk (2009) found that female T. oceanicus The reduction in genetic diversity (AR and expected from island populations, particularly Hawaii, were less heterozygosity) in eastern relative to western (Australian discriminating in their mating interactions than females and Pacific) populations (Table 4) could indicate recent from mainland Australian populations, a pattern consis- population size reductions, consistent with bottlenecks. tent with Kaneshiro’s effect (Kaneshiro, 1989) in which We found evidence of bottlenecks in seven populations bottlenecks select for less choosy females. In no-choice under the infinite alleles model (Table 1). Notably, we mating trials, a larger proportion of females from islands

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mated with silent flatwing males than did females from References Australia, suggesting these relaxed mating requirements might have facilitated the rapid evolutionary loss of the Addison, D.J. & Matisoo-Smith, E. 2010. Rethinking Polynesian crickets’ sexual signal in Hawaii (Tinghitella & Zuk, Origins: a West-Polynesia Triple-I Model. Archaeol. Oceania. 45: 2009). Until now, however, there was no evidence that 1–12. genetic bottlenecks did indeed occur upon the coloniza- Austerlitz, F., Jung-Muller, B., Godelle, B. & Gouyon, P.-H. tion of Pacific islands. The likelihood of bottlenecks upon 1997. Evolution of coalescence times, genetic diversity and colonization of the Hawaiian populations uncovered here structure during colonization. Theor. Pop. Biol. 51: 148–164. Austin, C.C. 1999. Lizards took express train to Polynesia. Nature provides the basis on which such changes in female 397: 113–114. mating requirements could occur. Barton, N.H. & Slatkin, M. 1986. 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