GENETICS Multi-Island Endemicity: Phylogeography and Conservation of Coelus pacificus (Coleoptera: Tenebrionidae) Darkling on the California Channel Islands

1,2 1 3 STYLIANOS CHATZIMANOLIS, LEIGH A. NORRIS, AND MICHAEL S. CATERINO Downloaded from https://academic.oup.com/aesa/article/103/5/785/10857 by guest on 30 September 2021 Ann. Entomol. Soc. Am. 103(5): 785Ð795 (2010); DOI: 10.1603/AN10037 ABSTRACT The California Channel Islands have been the focus of multiple conservation studies on charismatic vertebrates and plant species, but very few studies have focused on . In this study we examined the phylogeography of Coelus pacificus Fall (Coleoptera: Tenebrionidae), a dune- inhabiting darkling , endemic to the islands. Our aim in this study is to decipher the relationships between C. pacificus and the congeneric species Coelus ciliatus Eschscholtz that is distributed on the mainland, to examine the biogeographic relationships of the islands and augment the conservation efforts on the islands with data. We sequenced 235 specimens of Coelus for the cytochrome oxidase I mitochondrial gene. We performed phylogenetic analyses to assess the historical relation- ships of the different species and islands. We also examined the connectedness of the islands by using pairwise ⌽st and hierarchical analysis of molecular variance to test alternate hypotheses of geograph- ical structure. Based on the phylogenetic analyses, C. pacificus is a valid, multi-island endemic species. Haplotypes were grouped into two clades: one clade composed of Santa Cruz, Santa Rosa, San Miguel, and San Nicolas; and the other clade composed of Santa Catalina and San Clemente. The highest haplotypic diversity was observed in San Clemente and San Nicolas islands, but all islands had unique haplotypes. Two haplotypes morphologically indistinguishable from C. pacificus formed a sister clade to C. ciliatus, suggesting either an ancient hybridization event or cryptic speciation. The California Channel Islands should be managed on a system wide basis, at least for some of the organisms or habitats and each islandÕs population requires separate management to protect genetic integrity.

KEY WORDS Coleoptera, conservation genetics, island relationships, multi-island endemic, Tenebrionidae

Islands hold a key role in studies on evolutionary group of eight islands off the coast of southern Cali- (Gillespie and Roderick 2002) and conservation biol- fornia, have attracted considerable attention from ogy (Whittaker 1998, New 2008). The Galapagos and conservation biologists. However, the targets of these Hawaiian islands are prime examples of oceanic is- efforts have been almost entirely plants and verte- lands having a plethora of insect endemics (Howarth brates. The insect faunas of these islands, despite and Ramsay 1991, DeSalle 2001, Funk and Wagner showing considerable endemicity, are still poorly 2001) that currently face severe extinction threats due known and have not attracted signiÞcant conserva- to invasive and plants (Gurevitch and Padilla tion efforts. 2004, Causton et al. 2006, Liebherr and Kruschelnycky The California Channel Islands have been tradi- 2007) and habitat loss (Gagne´ 1988). Chown et al. tionally divided into northern (San Miguel, Santa (2008) also have documented the impact of climate Cruz, Santa Rosa, and Anacapa) and southern (San change on the insect faunas of southern oceanic is- Nicolas, Santa Barbara, San Clemente, and Santa lands. Mediterranean island systems have served as Catalina) groups (Fig. 1). The geological history of the models for assessing conservation risk due to over- islands is not clear. The Þrst emergence of island population and , where insects such masses occurred in the Miocene (17Ð13 MYA; Hall as butterßies and darkling beetles have Þgured prom- 2002), whereas most of the islands as known today inently (Dennis et al. 2008, Fattorini 2008, Dapporto were uplifted in the Pliocene between 5Ð2.5 MYA and Dennis 2009). The California Channel Islands, a (Hall 2002). Jacobs et al. (2004) indicated that due to the movement of the PaciÞc plate, early island masses 1 Department of Biological and Environmental Sciences, University rotated away from the San Diego area to their current of Tennessee at Chattanooga, 615 McCallie Ave., Department 2653, position between 17 and 12 MYA. Ward and Valensise Chattanooga, TN 37403. (1994, 1996 cited in Jacobs et al. (2004) hypothesized 2 Corresponding author, e-mail: [email protected]. 3 Department of Invertebrate Zoology, Santa Barbara Museum of that terrace deposits in Palos Verde peninsula and San Natural History, 2559 Puesta del Sol Rd., Santa Barbara, CA 93105. Nicolas island strongly suggest that their Þrst emer-

0013-8746/10/0785Ð0795$04.00/0 ᭧ 2010 Entomological Society of America 786 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 103, no. 5 Downloaded from https://academic.oup.com/aesa/article/103/5/785/10857 by guest on 30 September 2021

Fig. 1. Map of the California Channel Islands showing the location of unique haplotypes of C. pacificus. Squares correspond to haplotype CP1 that is shared between Santa Cruz and Santa Rosa. Stars indicate the location of haplotypes CP8 and CP9 on San Nicolas island. See text for details. gence from the sea was only Ϸ1 MYA. San Nicolas, that the remote location and the ownership status of most of San Miguel, Anacapa, and Santa Barbara were most of the islands would protect them from human thought to be completely resubmerged 0.5 MYA (Ved- impact, most islands face or faced in the recent past der and Howell 1980). Finally, during the last glacial extreme human environmental pressures. Numerous maximum (18,000Ð17,000 YA) when the sea level introduced species of vertebrates (e.g., feral goats, dropped considerably, the northern Channel Islands deer, elk, pigs, sheep, and even bison) and plants were united into one land mass (Santarosae) that was (European grasses, fennel [Foeniculum vulgare only 6 km from the mainland (Wenner and Johnson Miller], and ice plant [Carpobrotus edulis (L.)] are 1980). In the past, it has been hypothesized that the among the worst) and historic cattle and sheep ranch- islands had a land bridge with the mainland (based ing have all taken their toll (Powell 1994, Junak et al. mainly on some surprising faunal elements, e.g., mam- 1995, Wetterer et al. 2000, Knowlton et al. 2007, Ram- moths) but the underwater topography of the Santa sey et al. 2009). Many of these threats have been or are Barbara Channel is not consistent with any emergent being eliminated, especially the feral grazers, but connection (Junger and Johnson 1980, Wenner and many remain. Although actual human use of the is- Johnson 1980). lands remains very low, the impacts on many islands Management of the Channel Islands is complex. have not been critically evaluated. Most of the islands are currently administered by Complex geopolitical factors make conservation Channel Islands National Park (CINP). These include and restoration ecology choices on the California Santa Rosa, Santa Cruz, Anacapa, San Miguel and Channel Islands difÞcult. Any decision to be effective Santa Barbara. Santa Cruz Island is jointly managed by must be adopted by all parties involved and any con- CINP and , whereas San servation effort that affects species distributed on all Miguel Island is owned by the U.S. Navy but admin- islands must be coordinated with all aforementioned istered by CINP. The U.S. Navy has large military organizations. The current conservation effort on the installations on two islands, San Clemente and San islands is focused on a few charismatic vertebrates Nicolas, and access to these islands is restricted. Santa (Pergams et al. 2000, Roemer and Wayne 2003, Eggert Catalina is the only island with a permanent civilian et al. 2004, Delaney and Wayne 2005, Kohlmann et al. population and is a popular tourist area, but a large part 2005, Millus et al. 2007) and plants (Furches et al. 2009, of the island is managed by the Catalina Island Con- McEachern et al. 2009, Wallace and Helenurm 2009), servancy (CIC). Even though it seems on the outset whereas the insect fauna remains largely ignored. September 2010 CHATZIMANOLIS ET AL.: MULTI-ISLAND ENDEMICITY OF C. pacificus 787

However, any large-scale habitat conservation deci- the genus, and based on principal component analysis sions need to consider insect populations (Fonseca (PCA) of morphometric data argued that C. pacificus 2009), because many vertebrate or plant umbrella was adequately separated from other species, but a species (Lambeck 1997) do not adequately reßect study of the historical relationships of these species insect distributions and habitat needs (Kerr 1997, Ru- was not undertaken. More recently, Chatzimanolis binoff 2001). Very little is known about the status of and Caterino (2008) studied the phylogeography of C. insect species on the California Islands or about the ciliatus but the sample of C. pacificus that was used was potential threats they face. Powell (1994) and Ru- insufÞcient to make conclusions about their relation- binoff and Powell (2004) have studied the distribution ship. In general, multi-island endemic species are few patterns of moths on the islands, and Miller and Miller on the Channel Islands. Most endemic species are (1985) gave a detailed record of beetles on Santa single island endemics that are minimally differenti- Barbara island. More recently, M.S.C. et al. (in prep- ated from species on the mainland or on other islands aration) studied the distribution patterns and phylo- (Miller 1985). Most of those that do occur on multiple Downloaded from https://academic.oup.com/aesa/article/103/5/785/10857 by guest on 30 September 2021 geography of four beetles on the California Channel islands are distributed on multiple northern or south- Islands. However, our current collecting efforts ern islands, but rarely both (Miller 1985). Further- (M.S.C. et al., unpublished) have revealed dozens of more, studies of other beetle species have shown that beetle species not previously documented from the the northern islands and many of the southern islands islands with unknown conservation status. could have been colonized independently from main- To augment the conservation discussion on the Cal- land sources (M.S.C. et al., in preparation) and that ifornia Channel Islands with insect data from island the islands as a whole do not seem to function as a endemics, we investigated the phylogenetic and bio- biogeographic unit. C. pacificus, as a putative multi- geographic relationships in the Channel Island en- island endemic allows us to examine the potential demic Coelus pacificus Fall (Coleoptera: Tenebrion- biogeographic unity of the Channel Islands directly. idae). The genus Coelus includes Þve ßightless In this article, we address the following questions: fossorial beetle species distributed along the PaciÞc Are C. ciliatus and C. pacificus reciprocally monophy- Coast of from British Columbia, Can- letic? How are they related? Is C. pacificus a true ada, to Baja California, Mexico. All species of Coelus multi-island endemic? What is the pattern of coloni- live underneath plants in sand dunes. Coelus maritimus zation of the islands for C. pacificus? How closely Casey is distributed on the coast of Baja California and related are the different island populations? In addi- Blaisdell is found in relictual inland tion, we are interested in what are the implications for sand dunes of CaliforniaÕs inner coast ranges. Coelus island conservation based on the biogeographic pat- globosus LeConte and Coelus ciliatus Eschscholtz are terns observed in C. pacificus. both distributed on PaciÞc coast dunes. But Doyen (1976) suggested that C. globosus has a high tolerance Materials and Methods to saltwater immersion and hypothesized that this is why it is found on all islands except San Clemente. C. Taxon Sampling and Data Collection. C. ciliatus was ciliatus however, has less tolerance for saltwater sampled from Bodega Bay in northern California to (Doyen 1976) and is not found on any of the islands, San Diego in southern California. Chatzimanolis and with the possible exception of Anacapa (this record is Caterino (2008) examined the phylogeographic rela- poorly documented; Doyen 1976). Doyen hypothe- tionships of C. ciliatus and detailed sampling informa- sized that C. globosus might have colonized the islands tion can be found there. C. globosus was sampled from while the islands were connected to the mainland, but Santa Cruz and San Nicolas Islands and the mainland the current scenario for the geological history of the (San Onofre, Orange County), and C. gracilis from the islands suggest that they were never connected to the Monvero Dunes (Fresno County). We sampled C. mainland since their last emergence from the ocean pacificus from all islands except Santa Barbara and (Wenner and Johnson 1980). Doyen also suggested Anacapa (Fig. 1; Table 1). Even though we visited all that some colonization might have occurred through of the Channel Islands, we were unable to Þnd any rafting, a process witnessed for several animals Coelus on the last two islands. Our access to both (Schoenherr et al. 2003). C. globosus and C. gracilis are islands was rather restricted due to habitat closures for listed as species of special concern in California seabird or marine mammal breeding. Fall (1901) men- (CNDDB 2007) and in the past C. pacificus also was tioned a specimen of C. pacificus from Santa Barbara proposed to be included in that list. island, but Doyen (1976), in his extensive study of the C. pacificus is a multi-island endemic species and genus, did not examine any specimens from the island. until now its relationships to other congeneric species Santa Barbara islandÕs shores are extremely rocky and has not been clear. Until the revision of Doyen (1976), the overall available dune habitat seems limited for C. another species of Coelus (Coelus remotus Fall) was pacificus. Anacapa islands is composed of three sepa- recognized as valid (Blaisdell 1919) on San Clemente rate islands (west, central, and east), and we were island, but Doyen synonymized it with C. pacificus. granted limited access only to the eastern island where Strictly based on morphological characters, distin- no C. pacificus were found. We were not able to sample guishing C. pacificus and C. ciliatus (shape of frons and the Mexican species C. maritimus. clypeus; cranial punctation patterns) can be difÞcult. All specimens were collected in 100% ethanol and Doyen (1976) studied the biology and systematics of stored at Ϫ70ЊC. DNA voucher specimens are depos- 788 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 103, no. 5

Table 1. Population and locality information for C. pacificusa

Population Coordinates N Haplotypes San Miguel 15 6: CP32(10), CP33, CP34, CP35, CP36, CP37 Cuyler Harbor 34.0460Њ N, 120.3515Њ W 5 CP32(4), CP33 San Miguel Hill 34.0420Њ N, 120.3772Њ W 5 CP32(3), CP36, CP37 Simonton Cove 34.0628Њ N, 120.3735Њ W 5 CP32(3), CP34. CP35 Santa Rosa 15 6: CP1(10), CP27, CP28, CP29, CP30, CP31 OfÞcers Beach 33.9094Њ N, 120.0936Њ W 3 CP1(3) Dunes near Bee Canyon 33.9577Њ N, 120.1973Њ W 3 CP1(2), CP28 Southeast Anchorage 33.9797Њ N, 119.9990Њ W 2 CP1, CP29 Upper Lobo Canyon 34.0053Њ N, 120.0901Њ W 2 CP1(2) Arlington Canyon 34.0053Њ N, 120.1762Њ W 2 CP30, CP31 Mouth Lobo Canyon 34.0194Њ N, 120.0965Њ W 3 CP1(2), CP27

Santa Cruz 14 4: CP1(8), CP24(4), CP25, CP26 Downloaded from https://academic.oup.com/aesa/article/103/5/785/10857 by guest on 30 September 2021 Coches Prietos 33.9689Њ N, 119.7070Њ W 3 CP1(3) Laguna Beach 33.9630Њ N, 119.7961Њ W 5 CP1, CP24(4), CP25 Christy Beach 34.0238Њ N, 119.8766Њ W 5 CP1(4), CP26 San Nicolas 14 9: CP2, CP3(3), CP4, CP5(2), CP6, CP7, CP8(3), CP9, CP10 ͓no named locality͔ 33.2716Њ N, 119.5250Њ W 1 CP6 Nick Town 33.2538Њ N, 119.4851Њ W 1 CP8 Northwest Dunes 33.2637Њ N, 119.5597Њ W 3 CP3(2), CP8 Sandspit 33.2276Њ N, 119.4364Њ W 3 CP7, CP9, CP10 Sissy Cove 33.2643Њ N, 119.4857Њ W 2 CP5(2) Southside Dunes 33.2263Њ N, 119.5151Њ W 1 CP8 Thousand Springs 33.2836Њ N, 119.5300Њ W 3 CP2, CP3, CP4 San Clemente 16 8: CP11, CP12(2), CP13(2), CP14, CP15, CP16, CP17, CP18(7) BUDS Beach 33.0282Њ N, 118.5875Њ W 6 CP11, CP12(2), CP13(2), CP14 Flasher Road Dunes 33.0045Њ N, 118.5775Њ W 7 CP18(7) West Cove 33.0165Њ N, 118.5958Њ W 3 CP15, CP16, CP17 Santa Catalina 15 5: CP19, CP20(6), CP21, CP22 (5), CP23 Ben Weston Beach 33.3680Њ N, 118.4812Њ W 8 CP20, CP22(5), CP23(2) Little Harbor 33.3857Њ N, 118.4740Њ W 6 CP19, CP20(4), CP21 WhiteÕs Landing 33.3926Њ N, 118.3705Њ W 1 CP20

a N indicates of the number of specimens sampled. The number in parentheses indicates the number of specimens with the same haplotypes. Note that this table includes haplotypes CP8 and CP9 that do not belong in the C. pacificus clade based on the phylogenetic analysis. ited at the Santa Barbara Museum of Natural History, and Bayesian phylogenetic analyses. Parsimony anal- and complete collection data are available from the yses were performed in PAUP 4.0b10 (Swofford 2002), California Beetle Project database at www.sbnature. with all bases weighted equally, heuristic search with org/calbeetles. Total genomic DNA was extracted us- tree bisection and reconnection branch swapping and ing DNeasy Tissue extraction kit (QIAGEN, Valencia, 1,000 replicates. The maximum likelihood models for CA). We ampliÞed the cytochrome oxidase I (COI) COI were calculated using jModelTest 0.1.1 (Posada by using primers C1-J-2183 and TL2-N-3014 (Simon et 2008) and MrModeltest2 (Nylander 2004) using al. 1994). The ampliÞcation proÞle for COI consisted AkaikeÕs information criterion. Bayesian analyses of an initial denaturation for 5 min at 94ЊC, 35 cycles were performed with MrBayes 3.1.2 (Huelsenbeck of:45sat94ЊC,30sat45ЊC and 1 min at 72ЊC; followed and Ronquist 2001), using two runs with 107 genera- by a 2-min Þnal extension at 72ЊC. For taxa that resisted tions, each having four Markov chains; heating equal ampliÞcation, we used Platinum Taq (Invitrogen, to 0.2; and sampling every 100 generations. To assess Carlsbad, CA), which signiÞcantly improved the per- burn-in we used the program AWTY (Wilgenbusch et formance of the reaction. Polymerase chain reaction al. 2004) as well as the convergent diagnostic tools in (PCR) products were puriÞed using ExoSAP-IT (USB, MrBayes. We also used statistical parsimony haplo- Cleveland, OH) or QIAquick PCR puriÞcation kit type networks (Templeton et al. 1987, Templeton and (QIAGEN). Sequencing was performed commercially Sing 1993), as implemented in TCS (Clement et al. by Macrogen Inc. (Seoul, Korea), and all fragments 2000) to further examine the haplotype relationships were sequenced in both directions. Sequences were within C. pacificus. The networks were estimated originally edited using Sequencher 4.8 (Gene Codes, based on the 95% reconnection limit between haplo- Ann Arbor, MI) or Geneious Pro 4.5.4 (Biomatters types. Ltd., Auckland, New Zealand) and then imported We examined the connectedness of the islands us- in Se-Al v2.0a11 (http://tree.bio.ed.ac.uk/software/ ing pairwise ⌽st with 16,002 permutations and a seal/) for initial manual alignment and Þnally ex- TrN93 ϩ⌫model (Tamura and Nei 1993), with an ␣ ported to Mesquite 2.71 (Maddison and Maddison value of 0.212, as estimated by Arlequin version 3.1.1 2009). Alignment of COI sequences was trivial be- (ExcofÞer et al. 2005). Arlequin also was used to ex- cause no indels were present. amine hierarchical analysis of molecular variance Analyses. To assess historical relationships within (AMOVA; ExcofÞer et al. 1992). These analyses were Coelus, basic patterns of island colonization, and re- used to test alternate hypotheses of geographical lationships between islands, we conducted parsimony structure. We tested several alternative hypotheses September 2010 CHATZIMANOLIS ET AL.: MULTI-ISLAND ENDEMICITY OF C. pacificus 789 for the grouping of the islands: Þrst we separated the mon haplotype for C. pacificus and is the only haplo- islands into a north and a south group (as deÞned type found on more than one island, being found on above); we also separated the islands into two groups both Santa Cruz and Santa Rosa. The highest diversity and progressively transferred islands from one group of haplotypes is found on San Nicolas with nine hap- to the other going from west (San Miguel) to east (San lotypes, whereas San Clemente island has eight hap- Clemente). lotypes. Santa Rosa and San Miguel islands each have six haplotypes, Santa Catalina Þve haplotypes, and Santa Cruz four haplotypes. Results Population Structure and Diversity of C. pacificus. Specimens were initially identiÞed to the corre- After examining the results of the phylogenetic anal- sponding species based on the morphological charac- ysis, we were faced with the dilemma whether to ters provided by Doyen (1976). We sequenced 235 include haplotypes CP8 and CP9 from the San Nicolas specimens of Coelus (138 C. ciliatus, 89 C. pacificus, island in the population level analyses. Even though Downloaded from https://academic.oup.com/aesa/article/103/5/785/10857 by guest on 30 September 2021 seven C. globosus, and one C. gracilis) for a total of 85 CP8 and CP9 are morphologically identical to C. haplotypes. Haplotypes were named CC1ÐCC43 for C. pacificus, based on the COI phylogenetic analyses they ciliatus, CP1ÐCP37 for C. pacificus, CGl1ÐCGl4 for C. do not belong in the C. pacificus clade. We ran the globosus, and CGr1 for C. gracilis. The corresponding population level analyses twice, once including and GenBank accession numbers (EU032419ÐEU032462, once excluding these haplotypes. Below, we present GU332547ÐGU332587) are listed on Supplemental Ta- the result excluding these haplotypes, and we discuss ble S1 (online only). COI sequences were 825 bp, with instances where the inclusion of these two haplotypes 229 variable and 191 parsimony informative sites. alter the results. Phylogeographic Structure. Under the best Þtting Gene ßow was signiÞcantly restricted among dif- HKYϩ⌫ model, Bayesian analysis produced 75001 ferent islands as indicated by the ⌽st values (Supple- trees after burn-in (Fig. 2). Parsimony analysis results mental Table S2 [online only]). All pairwise compar- (data not shown) were largely congruent with the isons except Santa RosaÐSanta Cruz produced Bayesian analysis, although less resolved. Besides C. signiÞcant results, indicating very limited migration gracilis and C. globosus, which were sister to C. pacifi- between the islands. These results were expected be- cus ϩ C. ciliatus, there were several clades supported cause there are no shared haplotypes between the by high posterior probabilities. First, all C. ciliatus islands, with the exception of haplotype CP1 between formed a monophyletic group that is composed of two Santa Cruz and Santa Rosa. The inclusion/exclusion of subclades: one subclade is composed of haplotypes haplotypes CP8 and CP9 did not inßuence whether distributed in northern California (from Bodega Bay ⌽st values were signiÞcant for comparisons involving to Big Sur), and the other subclade is composed of San Nicolas island. haplotypes from central and southern California (San We tried several AMOVA analyses with different Luis Obispo to San Diego), with the exception of island groupings to test alternate hypotheses for clus- haplotypes CC17 and CC41 that are found in northern tering of the islands. In the analyses that did not in- California. Second, all but two C. pacificus haplotypes clude haplotypes CP8 and CP9 the highest among formed a monophyletic group that has its distribution group variation, indicative of geographic structure on the California Channel Islands. Within that mono- among populations (90.75%) was observed when San phyletic group, there were two subclades: one is com- Clemente and Santa Catalina islands were placed in posed of haplotypes found on San Clemente and Santa one group and all other islands on another. The tra- Catalina islands and another of haplotypes found on ditional hypothesis of separating the islands into Santa Cruz, Santa Rosa, San Miguel, and San Nicolas “north” and “south” showed only 55.43% among group islands. Third, two haplotypes (CP8 and CP9) from variation. All other possible groupings of islands had San Nicolas island formed a monophyletic group that even lower among group variation. Inclusion of hap- is the sister group to the clade containing the C. cili- lotypes CP8 and CP9 in the AMOVA analyses did not atus. Specimens with haplotypes CP8 and CP9 look alter drastically the results, it simply lowered the morphologically indistinguishable from C. pacificus, among group variation percentage. In the Þrst in- and their possible evolutionary history is discussed stance when comparing Santa Catalina and San Clem- below. ente against all other islands, the among-group vari- TCS produced four separate haplotype networks at ation was 79.54%, whereas in the “north” and “south” the 95% reconnection limit (Fig. 3) for C. pacificus. comparison the among group variation was 48.96%. One network is composed solely of haplotypes from San Clemente, another only of haplotypes from San Discussion Clemente and Santa Catalina, and another with hap- lotypes CP8-CP9. Finally, the largest network is com- In this article, we presented a comprehensive phy- posed of haplotypes from Santa Rosa, Santa Cruz, San logenetic analysis of the species of Coelus occurring in Miguel, and San Nicolas. In this network, haplotypes California. Based on our results the mainland species from San Miguel and San Nicolas are for the most part C. globosus, C. gracilis and C. ciliatus are all clearly isolated from other islandsÕ haplotypes, whereas hap- separated from C. pacificus, the endemic island spe- lotypes from Santa Rosa and Santa Cruz are scattered cies. Our results strongly support C. pacificus as a valid through the network. Haplotype CP1 is the most com- species. The monophyly of C. pacificus and by exten- 790 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 103, no. 5 Downloaded from https://academic.oup.com/aesa/article/103/5/785/10857 by guest on 30 September 2021

Fig. 2. Bayesian phylogenetic tree of nonredundant haplotypes for Coelus by using the HKYϩ⌫ model and midpoint rooting. Asterisk (*) indicates posterior probability Ն0.95. sion the function of the California Channel Islands as with remote mainland relationships, for example, the a single biogeographical unit is a rather unexpected lepidopterous fauna of the relictual island endemic outcome because multi-island endemicity, par- ironwood (Lyonothamnus floribundus Gray) (Miller ticularly spanning both the “northern” and “southern” 1985, Powell 1994). California Channel Islands is quite rare (Miller 1985). Our analyses of C. pacificus divided the California What multi-island endemics there are virtually never Channel Islands into two major groups: one group have close relatives on the adjacent mainland. They consisted of the “northern” islands plus San Nicolas are often related to either desert taxa or are relicts and the other group of San Clemente and Santa September 2010 CHATZIMANOLIS ET AL.: MULTI-ISLAND ENDEMICITY OF C. pacificus 791 Downloaded from https://academic.oup.com/aesa/article/103/5/785/10857 by guest on 30 September 2021

Fig. 3. Haplotype network for C. pacificus by using the 95% reconnection limit. Lines indicate one mutational step and haplotype numbers match those in the Bayesian tree.

Catalina. These groupings were corroborated both by types, a pair (CP30, CP31) from Santa Rosa especially the historical analyses (TCS and phylogenies) and the appeared as sister to all other haplotypes in the clade AMOVA. The grouping of Santa Cruz, Santa Rosa, and consisting of the northern islands and San Nicolas. C. San Miguel is well established in the literature for pacificus beetles occur in very large populations, and many different organisms (Ramirez and Beckwitt the retention of multiple lineages of haplotypes should 1995, Landry et al. 1999, Jockusch and Wake 2002, be consistent with this. Coyer et al. 2008) and reßects the common geological The close relationship of these northern island hap- history of these islands as “Santarosae.” Populations of lotypes to those on San Nicolas was very surprising. C. pacificus on each of these islands did not seem to be Although most haplotypes on San Nicolas are closely monophyletic with the exception of the San Miguel related to each other, they were only a single mutation population. For the CP1 haplotype shared by Santa from two on the northern islands, suggesting quite Cruz and Santa Rosa islands, we cannot be sure recent colonization of San Nicolas from the north. This whether this represents retention of ancestral poly- pattern, however, is proving to be quite common in morphism or ongoing gene ßow. Population level anal- phylogeographic studies, although it has not been yses did not Þnd restricted gene ßow between these widely recognized (Landry et al. 1999; Rubinoff and two islands. However, the commonness of haplotype Powell 2004; Ashley and Wills 1989; Coyer et al. 2008; CP1, broad distribution on both islands, and direct M.S.C. et al., in preparation). This fact alone would be relationship to other haplotypes on both islands sug- consistent with its relatively recent (Ͻ500,000-yr) in- gest that it may be ancestral. If there were signiÞcant undation and emergence (Vedder and Howell 1980). gene ßow between these islands, sharing of other However, the presence of the extremely divergent haplotypes would be expected. Both Santa Cruz and CP8 and CP9 (discussed below) lineage of C. pacificus Santa Rosa supported some fairly divergent haplo- on San Nicolas is much harder to explain. 792 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 103, no. 5

The second well supported island grouping is that of globosus are sympatric for at least part of their range San Clemente and Santa Catalina islands. This is sur- in southern California, and C. pacificus is sympatric prising given that these islands were never connected with C. globosus on most islands; so, presumably if no to each other, but there are other documented exam- reproductive barriers were there, hybridization would ples (Mahoney et al. 2003, Coyer et al. 2008), sup- have been observed in other instances. porting relationships between them. In addition, our The diversity of haplotypes on San Nicolas and San results suggest that there was one dispersal event of C. Clemente islands is in many respects unexpected. pacificus from Santa Catalina to San Clemente island These islands had the highest number of unique hap- (the CP11 and CP13 lineage; Figs. 2 and 3), which lotypes for C. pacificus among all islands sampled. It is must have occurred through some sort of rafting. Raft- worth mentioning here that all haplotypes found on ing on ßoating terrestrial debris has been observed in San Clemente were collected on the northern part of the past for several animals on the California Channel the island because the southern part is a restricted area

Islands (Schoenherr et al. 2003), and it also well es- due to U.S. Navy activity. The condition of the dunes Downloaded from https://academic.oup.com/aesa/article/103/5/785/10857 by guest on 30 September 2021 tablished for other oceanic systems (Holzapfel and and presence of C. pacificus in the southern part of the Harrell 1968). Another possible explanation is sea- island are uncertain. Based on the haplotype diversity surface (pleuston) transport (Peck 1994), and there is patterns seen on other islands (Fig. 1), we could hy- at least one documented case of sea-surface transport pothesize that the overall diversity of C. pacificus in of a (Phaleria manicata Boheman; Peck San Clemente is (or was) much higher than what we 1994). sampled. San Nicolas had the highest levels of haplo- Our recent work (M.S.C. et al., in preparation) on typic diversity for other beetle taxa, as well (M.S.C. et other beetle taxa [Hadrotes crassus (Mannerheim), al., in preparation). The high levels of haplotypic di- Hypocaccus lucidulus (LeConte), Nyctoporis carinata versity in San Nicolas are hard to explain considering LeConte, and Thinopinus pictus LeConte] on the Cal- that it presumably emerged for the Þrst time from the ifornia Islands has indicated multiple dispersal events sea 1 MYA (Ward and Valensise 1994, 1996) and was from the mainland to the islands and possible back completely resubmerged 0.5 MYA (Vedder and How- dispersal to the mainland from the islands as well. We ell 1980). If we accept this geological scenario as cor- originally expected that haplotypes of C. pacificus from rect, then populations on the island either diversiÞed different islands would intermingle with haplotypes of very quickly or were introduced from another island C. ciliatus from the nearby mainland, as it is the case that is currently submerged. for haplotypes between islands and mainland for other Perhaps one of the strongest messages produced by coastal beetle taxa. However, this is not the case here, this study is the need to consider conservation on the because all haplotypes of C. pacificus (with the ex- California Channel Islands on a system-wide basis, at ception of haplotypes CP8 and CP9) formed a mono- least for some of the organisms or habitats. C. pacificus phyletic group that is found only on the islands. had unique haplotypes on every island and other Among beetles examined to date, all except H. lucidu- multi-island endemics may show similar patterns. This lus are ßightless like C. pacificus, so the differences in situation may be compared with that of the Island Fox their biogeographical patterns cannot be explained [Urocyon littoralisi (Baird)] with distinct populations based on the presence of wings. H. crassus and T. pictus on each island. There each islandÕs population has are predators that live under beach wrack, presumably required separate management to protect genetic in- with high salt water tolerance, and this ability prob- tegrity. The California Channel Islands are currently ably facilitated more dispersal events than possible for administered by a number of organizations so estab- C. pacificus. lishing common goals and conservation practices One of the most intriguing results presented here is would be challenging. In the case of C. pacificus, pre- the presence of a clade comprised of haplotypes CP8 serving the ephemeral dune habitats should be of high and CP9 as the sister group to the clade of C. ciliatus. priority and to some extent this is happening in areas These haplotypes are found only on San Nicolas island where the threatened snowy plovers nest (Lafferty et and the beetles themselves are morphologically indis- al. 2006). However, in several islands the dunes extend tinguishable from C. pacificus. One possible explana- further inland where the snowy plovers are not found. tion for the presence of this clade is an ancient hy- In many such areas, invasive plants are coming to bridization event between C. pacificus and C. ciliatus. dominate dunes, and Coelus on the mainland is C. ciliatus has only been reported from Anacapa island, strongly negatively impacted by invasive dune plants so it is unclear how this could have happened. But (Slobodchikoff and Doyen 1977) In general, verte- perhaps ancient dispersals of C. ciliatus left mitochon- brates are not going to be adequate conservation in- drial DNA (mtDNA) that has been retained in C. dicators for insects such as C. pacificus, due to differ- pacificus. It is also conceivable that this highly distinct ences in dispersal and habitat use. Beyond the lineage represents a cryptic species (5.6% uncorrected implications for island endemics, off-shore islands distance from any C. ciliatus; Ͼ8% from any other C. have an important role for the conservation of main- pacificus). Unfortunately, mtDNA alone cannot an- land species (Sugiura et al. 2009). Several beetles that swer such questions and data from nuclear genes are were known to be historically common on the main- needed to examine these hypotheses. Although there land have recently been found only on the islands are no data on the presence of reproductive barriers (M.S.C., unpublished data). Therefore, preserving the in Coelus, such barriers must exist. C. ciliatus and C. habitat on the islands serves both island and mainland September 2010 CHATZIMANOLIS ET AL.: MULTI-ISLAND ENDEMICITY OF C. pacificus 793 species. We are hopeful that this and other studies on Dennis, R.L.H., L. Dapporto, T. G. Shreeve, E. John, J. G. insect island endemics would promote a further un- Coutsis, O. Kudrna, K. Saarinen, N. Ryrholm, and W. R. derstanding of the biodiversity of the California Chan- Williams. 2008. Butterßies of European islands: the im- nel Islands and push the current conservation efforts plications of the geography and ecology of rarity and toward a more holistic approach. endemicity for conservation. J. Insect Conserv. 12: 205Ð 236. DeSalle, R. 2001. Molecular approaches to biogeographic Acknowledgments analysis of Hawaiian Drosophilidae, pp. 72Ð89. In W. L. Wagner and V. A. Funk [eds.], Hawaiian biogeography. We are grateful to numerous biologists and land managers Evolution on a hot spot archipelago. Smithsonian Insti- for assistance with collecting specimens for this study, espe- tution, Washington, DC. cially Maxi Polihronakis, Katie Hopp, Kate Faulkner, Sarah Doyen, J. T. 1976. Biology and systematics of the genus Chaney, Carolyn Greene, Grace Smith, Darcee Gutilla, Lyn- Coelus (Coleoptera: Tentyriidae). J. Kans. Entomol. Soc. dal Laughrin, Melissa Booker, Peter Hammond, Lon Otterby, 49: 595Ð624. Downloaded from https://academic.oup.com/aesa/article/103/5/785/10857 by guest on 30 September 2021 Sandy Gifford, Michael Walgren, Lisa Adreano, and Cristina Eggert, L. S., N. I. Mundy, and D. S. Woodruff. 2004. Pop- Sandoval. We would also like to thank Michael Westphal for ulation structure of loggerhead shrikes in the California his help with Coelus gracilis. For Þeld assistance and collect- Channel islands. Mol. Ecol. 13: 2121Ð2133. ing permissions, we are also grateful to the Bodega Bay Excoffier, L., P. E. Smouse, and J. M. Quattro. 1992. Analysis Marine Laboratory, BLM, the Channels Islands National of molecular variance inferred from metric distances Park, the California State parks, the California Department of among DNA haplotypes: application to human mitochon- Fish and Game, the Catalina Island Conservancy, the Nature drial-DNA restriction data. Genetics 131: 479Ð491. Conservancy, the U.S. Navy, the Department of the Navy on Excoffier, L., G. Laval, and S. Schneider. 2005. ARLEQUIN behalf of the Naval Base Coronado, San Clemente Island ver. 3.0: an integrated software package for population Naval Auxiliary Landing Field, and the University of Cali- genetics data analysis. Evol. Bioinform. Online 1: 47Ð50. fornia Natural Reserve System. We gratefully acknowledge Fall, H. C. 1901. List of the Coleoptera of southern Cali- the assistance of Gretchen Betzholtz and Iliana Ouzounov in fornia, with notes on habits and distribution and descrip- the laboratory. 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