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Connectivity and Molecular Ecology of Antarctic Fishes

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Connectivity and Molecular Ecology of Antarctic Fishes Chapter 5 Connectivity and Molecular Ecology of Antarctic Fishes Filip A. M. Volckaert, Jennifer Rock and Anton P. Van de Putte 5.1 Introduction The international program on Evolution and Biodiversity in the Antarctic (Anonymous 2005) focused on the influence of evolution and diversity of life on the properties and dynamics of the Southern Ocean (SO) biome. It also wanted to predict how communities and organisms respond to environmental change. A component of the program aimed at understanding micro-evolutionary processes and dynamics during the Pleistocene and Holocene. The past three million years have shaped the ‘‘shallow’’ evolution of genes, organisms and ecosystems through major climate changes and short period earth periodicities. Fish, a major source of ecosystem goods, play a key role in the ecosystem. However, it is only since relatively recently that the fish communities of the SO started to reveal their characteristics. Before summarizing the current understanding of their connec- tivity and molecular ecology, we introduce the reader to those aspects that have affected their recent evolution so much. F. A. M. Volckaert (&) Á A. P. Van de Putte Laboratory of Biodiversity and Evolutionary Genomics, Katholieke Universiteit Leuven, Charles Deberiotstraat 32, 3000 Leuven, Belgium e-mail: fi[email protected] J. Rock Department of Zoology, University of Otago, Dunedin 9054, New Zealand e-mail: [email protected] A. P. Van de Putte Belgian Biodiversity Platform, Royal Belgian Institute for Natural Sciences, Vautierstraat 27, 1000 Brussels, Belgium e-mail: [email protected] G. di Prisco and C. Verde (eds.), Adaptation and Evolution in Marine Environments, 75 Volume 1, From Pole to Pole, DOI: 10.1007/978-3-642-27352-0_5, Ó Springer-Verlag Berlin Heidelberg 2012 76 F. A. M. Volckaert et al. A most outstanding observation is that environmental conditions at high latitudes are extreme. The water temperature hovers amazingly stable close to the freezing point and has high oxygen saturation values (see Chap. 8 Marshall 2012). Local fish species have adapted to these conditions through amongst others slow metabolism, restricted thermal tolerance (Pörtner 2006), long generation times, above average values of blood osmolarity through lacing with anti-freeze proteins (see Chap. 8 Marshall 2012) and the loss of gene functions, e.g. heat shock and hemoglobin (di Prisco et al. 2002; see Chap. 11 Verde et al. 2012). The strong seasonal photoperiod leads to time-constrained primary production with the microbial loop playing an important role throughout the year (Thomson et al. 2010). Also the conditions of the SO proper are peculiar. The upper water column has been isolated from the world oceans for some 31 million years through the presence of a stable frontal system, the Antarctic Polar Front (APF) (Lawver and Gahagan 2003). South of the APF flows the Antarctic Circumpolar Current (ACC) clockwise around the Antarctic continent up to 2,000 m depth. It might favour large-scale dispersal of Antarctic organisms and lead to homogenised communi- ties. The physical and hydrodynamic continuity between ocean surface and bottom suggests continuity between the faunas of the surface waters and adjacent deep-sea (Gutt et al. 2010). On a regional scale the nearshore East Wind Drift and clockwise gyres (such as the Weddell and Ross Sea) may have lead to evolutionary isolation. The average depths of the continental shelves are larger than most shelves (500 m) and widths are rather narrow except for the large embayments in the Ross and Weddell Seas. Sea ice covers 60% of the continental shelf in winter and 20% in summer. In the past the continental ice mass has shaped the profile of the conti- nental shelf, especially through the recurrence of grounded ice during Glacial Periods (Thatje et al. 2005). Benthic biodiversity is locally very high, but unlike first thought not uniformly high (Gutt et al. 2010). Global change has been dramatic in the SO with the loss of many animal taxa since the Cenozoic (Rogers 2007). The disappearance of many fish taxa created new opportunities (niches) for the surviving taxa. Notothenioidea (129 species) and Liparidae expanded and diversified into novel habitats. Today the SO harbours a remarkably high (88%) level of endemism (Eastman 2005; Chap. 6 Lecointre 2012). Ancestral notothenioids had a demersal life-style and gradually colonized the water column. The absence of a swim bladder lead to alternative paths to neutral buoyancy, for example through lipid deposition and reduced skeletal mineralisation (Eastman and Barrera-Oro 2010; Patarnello et al. 2011). Pleistocene glaciations have led to the extrusion of continental shelf fauna during cold epochs and recolonisation from refugia during warm epochs (Thatje et al. 2005). As the shelves were narrow, taxa were forced either to occupy greater depths or to adapt a pelagic life-style. SO fish has stenothermal traits (Patarnello et al. 2011), which contrasts with the broader phenotypic plasticity of smaller and more active invertebrates (Peck et al. 2009). Although fish may acclimate up to 4°C (Bilyk and DeVries 2010), overall the current scale of change outpaces their evolutionary potential. Their typically long generation times do not allow fast adaptation. 5 Connectivity and Molecular Ecology of Antarctic Fishes 77 Considerable conceptual and technical progress have stimulated research on the ecosystems and biota of the SO. It includes the launching of ice-strengthened research vessels and satellites equipped with platforms for remote sensing, tools operational under extreme conditions, hydrodynamic models (Webb and de Cuevas 2007) and novel molecular approaches (see below). They all promoted our understanding of the recent evolution of the SO. 5.2 Patterns of Genetic Diversity in Past and Present Genetic diversity integrates as well historical events (the accumulation of muta- tions through expanding populations combined with systematic loss due to extinction of populations) as contemporary events of population migration and fitness (the potential to adapt). On average, marine populations have high genetic diversities because of high effective population sizes (and hence reduced chances for genetic drift and inbreeding). 5.2.1 Accessing Genetic Diversity Remarkable technological progress originating from the drive to supply affordable single genomes (1,000 US$ genome) has created new opportunities to study biological evolution (Clark et al. 2011). Low-density genotyping is increasingly complemented by high density and high-throughput genotyping and profiling. There are now suitable tools available for the correct estimation of genetic origin at the between and within species level. At the population level large numbers of individuals can be typed, regardless of size. The transition has lead to remarkable and unique outcomes. Here we list some of the realized and potential applications of genomic tools to screen populations of Antarctic fishes. Metagenomics, the analysis of the genomes of organisms recovered from the environment, started on picoplankton communities of the open ocean (Rusch et al. 2007). It is now generally implemented and used for screening prokaryotes and eukaryotes of complete biological communities (microbiome). Applications in the SO are in progress. An equally massive but more targeted approach is metage- netics, the en masse characterization of operational taxonomic units (OTU) at a single locus, for example the nuclear small subunit 18S (nSSU). Logical targets are soft bottom communities (Creer et al. 2010), but also plankton and fish qualifies. Ward et al. (2009) analyzed bacterial 16S rRNA gene sequences from the intes- tinal tract of Notothenia coriiceps and Chaenocephalus aceratus. Simple Sequence Repeats (SSRs) or DNA microsatellites, which are tandem repeats from one to five base pairs, have proven their usefulness in detecting contemporary patterns. Progress from the first microsatellites of notothenioids isolated with some diffi- culty from genomic DNA libraries (Reilly and Ward 1999; Susana et al. 2007; 78 F. A. M. Volckaert et al. Van Houdt et al. 2006; Van de Putte et al. 2009) to the current large scale mining of EST-SSRs (albeit not yet in fishes of the SO, but see Vogiatzi et al. 2011) has lead to more balanced genome-wide sampling and hence characterization of populations. However, SSRs suffer from poor standardization and transportability between platforms. Point mutations in the genome, known as Single Nucleotide Polymorphisms (SNPs), are the most common type of genetic marker (Brumfield et al. 2003). They have the advantage of being platform independent and hence standardized. Their genome wide occurrence has lead to quick acceptance (Kuhn and Gaffney 2008). Large-scale applications on fishes of the SO are under development. Outlier SNPs seem perfectly suitable to detect weak population structure, which is a most typical feature of marine populations (Nielsen et al. 2009). Also Copy Number Variation (CNV), although occurring at a lower frequency throughout the genome, harbours a high information content. Much is expected from the genotyping of complete genomes (Hohenlohe et al. 2010); it represents a major change in approach, as the full blueprint can be mined for information. Also, gene transcripts contain lots of information to understand genome evolution, population patterns and molecular physiology. Excellent high resolution and high throughput tools (from microarrays to next generation sequencing) are operational
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