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Historic Hybridization and Introgression Between Two Iconic Australian Anemonefish and Contemporary Patterns of Population Connectivity M

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Historic Hybridization and Introgression Between Two Iconic Australian Anemonefish and Contemporary Patterns of Population Connectivity M Historic hybridization and introgression between two iconic Australian anemonefish and contemporary patterns of population connectivity M. H. van der Meer12,G.P.Jones23, J.-P. A. Hobbs4 & L. van Herwerden1,2 1Molecular Ecology and Evolution Laboratory, Australian Tropical Sciences and Innovation Precinct, James Cook University, Townsville 4811, Australia 2School of Marine and Tropical Biology, James Cook University, Townsville 4811, Australia 3ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville 4811, Australia 4The Oceans Institute and School of Plant Biology, The University of Western Australia, Crawley 6009, Australia Keywords Abstract Amphiprion, coral reef fish, endemism, extinction risk, Great Barrier Reef, isolated Endemic species on islands are considered at risk of extinction for several reasons, islands, Lord Howe Island. including limited dispersal abilities, small population sizes, and low genetic diver- sity. We used mitochondrial DNA (D-Loop) and 17 microsatellite loci to explore Correspondence the evolutionary relationship between an endemic anemonefish, Amphiprion mccul- M. H. van der Meer, Molecular Ecology and lochi (restricted to isolated locations in subtropical eastern Australia) and its more Evolution Laboratory, Australian Tropical widespread sister species, A. akindynos.AmitochondrialDNA(mtDNA)phylogram Sciences and Innovation Precinct, James Cook University, Townsville 4811, Australia. showed reciprocal monophyly was lacking for the two species, with two supported Tel: +61 (07)4871 5423; groups, each containing representatives of both species, but no shared haplotypes E-mail: [email protected] and up to 12 species, but not location-specific management units (MUs). Population genetic analyses suggested evolutionary connectivity among samples of each species Funded by Australian Department of the (mtDNA), while ecological connectivity was only evident among populations of the Environment and Water Resources, and endemic, A. mccullochi. This suggests higher dispersal between endemic anemone- Envirofund Australia. fish populations at both evolutionary and ecological timeframes, despite separation Received: 19 February 2012; Accepted: 1 by hundreds of kilometers. The complex mtDNA structure results from historical March 2012 hybridization and introgression in the evolutionary past of these species, vali- dated by msat analyses (NEWHYBRIDS, STRUCTURE, and DAPC). Both species had high genetic diversities (mtDNA h > 0.90, π = 4.0%; msat genetic diversity, gd > 0.670). While high gd and connectivity reduce extinction risk, identifying and doi: 10.1002/ece3.251 protecting populations implicated in generating reticulate structure among these species should be a conservation priority. adaptive capacity of endemic species or isolated populations Introduction is required in order to understand what increases their risk of Remote islands often contain a disproportionate number of extinction, thereby enabling the development of appropriate endemic species (Ceballos and Brown 1995; Randall 1998; conservation measures (Faith 1992; Moritz 2002). Gillespie et al. 2008) and genetically distinct populations of Throughout the world’s tropical oceans, coral reef organ- species with broad geographic ranges (Avise 1992; Slatkin isms are distributed on islands and reefs that represent vary- 1993). The uniqueness of island communities makes them ing degrees of isolation. For coral reef fish, it is the most iso- a high conservation priority (Gillespie and Roderick 2002), lated locations that contain the highest levels of endemism even more so given the extremely high rates of local and global (Lessios et al. 2001; Jones et al. 2002; Allen 2008). Isolated extinctions of species inhabiting islands (Steadman 1995). islands also support genetically differentiated populations of Island endemics face an elevated risk of extinction because some widespread reef fish species (Muss et al. 2001; Planes they often have vulnerable traits, such as, limited dispersal and Fauvelot 2002; Winters et al. 2010). Islands communi- abilities, small population sizes, and low genetic diversity ties are also characterized by a high proportion of vagrants, (gd) due to genetic drift and inbreeding (Frankham 1997, which can result in a high incidence of hybridization due to a 1998). A sound knowledge of the evolutionary history and scarcity of conspecific mates (Hobbs et al. 2009b). Reef fish on c 2012 The Authors. Published by Blackwell Publishing Ltd. This is an open access article under the terms of the Creative 1 Commons Attribution Non Commercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. Historic Hybridization between Anemonefish M. H. van der Meer et al. isolated islands also appear to be more vulnerable to extinc- A. mccullochi are unknown. Amphiprion akindynos may be tion as evidence by recent extinctions (Roberts and Hawkins less of a conservation concern because it is more widely dis- 1999; Dulvy et al. 2003). These extinctions highlight the need tributed, inhabits six species of anemones (Fautin and Allen to examine the genetic characteristics of island fish faunas 1997), and can be locally abundant (e.g., Richardson 1999). to help determine why this group may be vulnerable. Pro- This study addressed the following specific questions: cesses that influence genetic resilience and promote species (1) What is the evolutionary relationship between the sis- persistence times may be identified by examining spatial and ter species, A. mccullochi and Aakindynos,basedonmito- temporal patterns of gene flow. chondrial DNA (mtDNA)? (2) How many management units Coral reef anemonefish (genus Amphiprion)representa (MUs, sensu Moritz 1994) can be identified for A. mccullochi useful model system for understanding evolutionary histo- and A. akindynos? (3) What is the contemporary relation- ries and population genetic structures of island fish faunas. ship of connectivity between and within species, based on Although the genus has a broad Indo–Pacific distribution, msat DNA? (4) What are the genetic diversities of these sis- more than 25% of species are endemic to isolated islands or ter species and do they suggest resilience or susceptibility to have peripheral populations at these remote locations (Fautin extinction and environmental change? Identifying MUs, in- and Allen 1997). Although these island endemics are often cluding the direction of connectivity between these units, is closely related to more broadly distributed sister species, the essential information to ascertain best practice management historic colonization and speciation processes, and current and maximize biodiversity conservation of these important levels of population differentiation are not well known. In a southernmost coral reefs. We discuss the implications of the detailed phylogenetic study of 23 of the 28 anemonefish, underlying genetic structure to extinction risk and the con- Santini and Polacco (2006) suggested the group (Family: servation of these remote populations. Pomacentridae, subfamily Amphiprioninae) originated some 5–13 million years ago in the Indo–Pacific, with many of the Materials and Methods endemics being of recent origin. A more detailed investiga- tion of their historic relationships with putative sister species, Study system and current levels of gene flow among locations, is necessary McCulloch’s anemonefish (A. mccullochi) has the smallest to understand how endemic anemonefish originate and per- geographic range of any of the 28 species of anemonefish sist. This information will be useful for predicting how these and is endemic to three isolated, oceanic locations more than species will persist in the future and aid management strate- 600 km off the east Australian coastline (ER, MR, and LHI). It gies aimed at conserving these iconic coral reef fish. is only found living in close association with its host anemone, Using phylogenetic and population genetic analyses, we E. quadricolor, andoccursatdepthsbetween2and45m reconstructed the evolutionary history of two Australian (Fautin and Allen 1992). Its coloration of black body with anemonefish: a small-range species, Amphiprion mccullochi a whitish snout, caudal peduncle, and caudal fin makes it (endemic to Middleton Reef [MR], Elizabeth Reef [ER], easily recognizable. Its sister species, A. akindynos (Santini andLordHoweIsland[LHI])anditsmorewidespreadsis- and Polacco 2006) is more widespread, ranging from the ter species, A. akindynos, found on the Great Barrier Reef, Great Barrier Reef (GBR) south to the Solitary Islands and New Caledonia and the subtropical east coast of Australia. extending out to New Caledonia (but not including ER and The endemic McCulloch’s anemonefish is of particular con- MR or LHI). It lives among its host anemones E. quadricolor, servation concern because it has three characteristics known Heteractis aurora, H. crispa, H. magnifica, Stichodactyla to elevate the risk of extinction—a very small geographic haddoni,andS. mertensii (Fautin and Allen 1992), at depths range (Coleman 1980; Fautin and Allen 1992; Hobbs et al. between 1 and 25 m (Allen 1991). It has two white bars on its 2009a), extreme habitat specialization (one species of host body and a color transition from a dark brown/orange body anemone—Entacmaea quadricolor; Fautin and Allen 1992) to a whitish caudal fin (Fautin and Allen 1992). and relatively small local populations (Choat et al. 2006; Hobbs
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