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ISSN 0025-3162, Volume 157, Number 6 ISSN 0025-3162, Volume 157, Number 6 This article was published in the above mentioned Springer issue. The material, including all portions thereof, is protected by copyright; all rights are held exclusively by Springer Science + Business Media. The material is for personal use only; commercial use is not permitted. Unauthorized reproduction, transfer and/or use may be a violation of criminal as well as civil law. Mar Biol (2010) 157:1357–1366 Author's personal copy DOI 10.1007/s00227-010-1415-7 ORIGINAL PAPER Phylogeography of the rock-pool copepod Tigriopus brevicornis (Harpacticoida) in the northern North Atlantic, and its relationship to other species of the genus Lisa Handschumacher · María Björk Steinarsdóttir · Suzanne Edmands · Agnar Ingólfsson Received: 19 April 2009 / Accepted: 18 February 2010 / Published online: 9 March 2010 © Springer-Verlag 2010 Abstract We investigated relationships among North Introduction Atlantic Tigriopus brevicornis populations and their rela- tionships to Mediterranean T. fulvus and North American Marine species with limited dispersal capacity are useful T. californicus, using crossing experiments and mitochondrial for the study of phylogeography, oVering potentially DNA sequencing. All T. brevicornis populations tested greater resolution in inferring current directions, dispersal were interfertile, while interspeciWc crosses produced either barriers and climatic history. The copepod genus Tigriopus no oVspring or oVspring that did not survive past the larval presents the counterintuitive combination of extremely stage, with the exception of a few T. brevicornis £ T. cali- restricted dispersal (e.g. Burton and Lee 1994) and wide fornicus crosses that produced mature adults. DNA geographic distribution (see below), making it possible to sequencing of a fragment of mitochondrial cytochrome oxi- test whether the same phylogenetic patterns are repeated in dase I (COI) showed that samples of T. brevicornis from distant regions. Because Tigriopus spp. are amenable to Iceland, the Faroes, Ireland, Scotland and Nova Scotia laboratory breeding experiments (e.g. Battaglia 1982; formed a single shallow clade. In contrast, T. brevicornis Edmands 1999), it also becomes possible to test whether from more southern populations in France and Portugal genetic patterns are concordant with reproductive patterns. formed a clade with substantially greater branch lengths. Tigriopus spp. are found on rocky shores nearly world- Tigriopus brevicornis was monophyletic, and T. brevicor- wide. They occur, for example, both on continents and on nis plus Mediterranean T. fulvus were together also mono- far oVshore islands such as Kerguelen, Crozet Islands and phyletic. The phylogeography of T. brevicornis closely South Georgia (Davenport et al. 1997). They are found mirrored that found in T. californicus, with substantially under extreme cold conditions on the Antarctic Peninsula reduced interpopulation divergence at northern latitudes. (Waller et al. 2006), under subtropical conditions in Mexico The known distribution of T. brevicornis in Iceland and the (Ganz and Burton 1995; Edmands 2001) and in tropical Faroes is shown and dispersal mechanisms and habitat conditions in Southern Asia (Jung et al. 2006; Ki et al. selection brieXy discussed. 2008). Tigriopus spp. are typically found in high shore splash-pools, although they are also known to occur subti- dally on the Antarctic Peninsula (Waller et al. 2006). Also, Lang (1948) mentions a unique record of Tigriopus brevi- Communicated by S. Uthicke. cornis at depth of 10 m oV the coast of Sweden. In the northern hemisphere, 6 species have been recognized (Dav- L. Handschumacher · S. Edmands (&) Department of Biological Sciences, enport et al. 1997). While the taxonomy in the southern University of Southern California, hemisphere is less well understood, there are at least 6 spe- Los Angeles, CA 90089, USA cies, not all of which have been described (e.g. Bradford e-mail: [email protected] 1967; Soyer et al. 1987; Davenport et al. 1997). To our M. B. Steinarsdóttir · A. Ingólfsson knowledge, sympatry of two or more species has not been Institute of Biology, University of Iceland, recorded in any location. In the northern North Atlantic, the Aragata 9, 101 Reykjavík, Iceland only species found appears to be T. brevicornis, with a 123 1358 Author's personal copy Mar Biol (2010) 157:1357–1366 known distribution ranging from Portugal in the south to primary questions we addressed were: (1) Does the popula- Iceland and Nova Scotia in the north (Ingólfsson and tion genetic structure of T. brevicornis in the northern Steinarsdóttir 2006). Its discovery in the Faroes, Iceland North Atlantic parallel that of T. californicus in the PaciWc? and Nova Scotia is recent and quite surprising (Ingólfsson and (2) What are the genetic and reproductive relationships of Steinarsdóttir 2006), but in all these regions, it is common, T. brevicornis intraspeciWcally and to T. californicus and being recorded from many localities. On the western coasts T. fulvus? Secondarily, we also wanted to determine whether of North America, T. brevicornis is replaced by T. califor- the habitat preferences of T. brevicornis in Iceland, where it nicus, and in the Mediterranean by T. fulvus, which has also has only recently been discovered, were similar to those been reported from the Atlantic Islands of Madeira (Daven- elsewhere. Finally, we wanted to investigate the possible port et al. 1997). Both of these species diVer morphologi- role of birds and Xoating algae as dispersal agents that cally in only minute details from T. brevicornis, which was could help explain the species’ wide distribution in the face only recently recognized as taxonomically distinct from of seemingly limited dispersal capacity. T. fulvus (Carli and Fiori 1977). On the western coasts of North America, it has been found that southern populations of T. californicus, in Materials and methods Mexico and California, may be quite genetically distinct from each other, while more northern populations, from Oregon Samples and distribution to Alaska, appear to be derived, with substantially lower interpopulation divergence (Edmands 2001). This has been We obtained samples from virtually the whole known dis- attributed to a more recent origin of the northern popula- tributional range of T. brevicornis, from Portugal in the tions, which cannot have settled in these northern regions south to Iceland and Nova Scotia in the north (Fig. 1). We until the ice retreated about 12–15 thousand years ago after also obtained samples of T. fulvus from the Mediterranean the last glacial maximum (Edmands 2001). The situation in coast of Spain. PaciWc animals were obtained from southern the North Atlantic parallels these conditions. During the California. Sampling locations are shown in Table 1. Speci- last glacial maximum, the ice shield reached as far south as mens were either preserved in ¸96% ethanol for mtDNA Britain and France, while the oVshore islands of the Faroes assays or brought alive to the laboratories of the Institute of and Iceland were with little doubt covered by separate ice Biology, University of Iceland or the Department of Bio- shields (e.g. Sejrup et al. 2005). Survival of Tigriopus spp. logical Sciences, University of Southern California, Los north of the edge of the ice shields is improbable. Angeles, for crossing experiments. Cultures were held at Here, we examined genetic and reproductive relation- 12°C and 12:12 d:l light regime in Iceland. In California, ships of T. brevicornis in the North Atlantic, using mito- cultures were held at 15 or 20°C under a light regime of chondrial DNA sequencing and crossing experiments. The 12:12 d:l. The animals were acclimatized to these condi- Fig. 1 Labeled localities pro- -60 -40 -20 0 vided Tigriopus brevicornis samples for the current study. Additional circles in the Iceland 65 inset indicate records of T. brev- icornis from 2003, when it was Wrst discovered, to 2008. Locali- ties are grouped into 10 £ 10 km squares (see Ingólfsson 1996). 60 Additional circles in the Faroes inset indicate records of T. brev- -19 -7 Ire1 Sco1 icornis from June 2004 Far1 55 62 Ice5 65 Faroes Ire2 Iceland 50 Ice2 Ice4 40 km Ice1 Fra1 Ice3 Ice6 Fra2 45 100 km Nov1 Nov2 40 400 km Por1 35 123 Mar Biol (2010) 157:1357–1366 Author's personal copy 1359 Table 1 Localities of Tigriopus brevicornis (TB), T. fulvus (TF) and T. californicus (TC) samples used in habitat studies, crosses and/or DNA sequencing Location Habitat Crosses Sequenced Latitude Longitude (no. samples) TB_Far1 Kunoy, Faroes X (3) 62°17.6Ј ¡6°40.2Ј TB_Fra1 Callot, France X X (2) 48°43.8Ј ¡3°59.9Ј TB_Fra2 Concarneau, France GenBank 47°52Ј ¡3°55Ј TB_Nov1 Parker’s Cove, Nova Scotia X X (5) 44°48.8Ј ¡65°32.2Ј TB_Nov2 Peggy’s Cove, Nova Scotia X X (1) 44°29.6Ј ¡63°55.0Ј TB_Ice1 Seltjarnarnes, Iceland X X 64°09.8Ј ¡22°00.6Ј TB_Ice2 Borgarnes, Iceland X (2) 64°32.1Ј ¡21°55.4Ј TB_Ice3 Hvaleyri, Iceland X (4) 64°03.7Ј ¡21°59.8Ј TB_Ice4 Hvalnes, Iceland X (2) 64°24.2Ј ¡14°32.4Ј TB_Ice5 Skagaströnd, Iceland X (1) 65°49.6Ј ¡20°19.4Ј TB_Ice6 Garðskagi, Iceland X X 64°05.1Ј ¡22°41.7Ј TB_Ire1 Malin Head, Ireland X 55°22Ј ¡7°20Ј TB_Ire2 Cork, Ireland GenBank 51°57Ј ¡8°40Ј TB_Sco1 Firth of Forth, Scotland X (2) 55°59.9Ј ¡3°23.9Ј TB_Por1 Sines, Portugal X X (2) 37°57.7Ј ¡8°55.3Ј TF_Fra3 Banyuls, France Edmands (2001) 42°28.9Ј 3°08.3Ј TF_Spa1 Tossa de Mar, Spain X 41°43.4Ј 2°56.2Ј TF_Spa2 Cala de Saint Fransesc, Spain X 41°40.7Ј 2°48,5Ј TF_Spa3 Blanes, Spain X Edmands
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