Multi-Island Endemicity: Phylogeography and Conservation of Coelus Pacificus (Coleoptera: Tenebrionidae) Darkling Beetles On
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GENETICS Multi-Island Endemicity: Phylogeography and Conservation of Coelus pacificus (Coleoptera: Tenebrionidae) Darkling Beetles 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 insects. In this study we examined the phylogeography of Coelus pacificus Fall (Coleoptera: Tenebrionidae), a dune- inhabiting darkling beetle, 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 insect 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 animals 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 invasive species, 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 the Nature Conservancy, 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.