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Diversification of Low Dispersal Crustaceans Through Mountain Uplift

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Diversification of Low Dispersal Crustaceans Through Mountain Uplift bs_bs_banner Zoological Journal of the Linnean Society, 2014, 170, 591–633. With 27 figures Diversification of low dispersal crustaceans through mountain uplift: a case study of Gammarus (Amphipoda: Gammaridae) with descriptions of four novel species ZHONGE HOU1, JUNBO LI2 and SHUQIANG LI1* 1Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China 2School of Life Science, Shanxi Normal University, Linfen 041000, China Received 22 July 2013; revised 21 November 2013; accepted for publication 23 November 2013 Lineages with low dispersal ability are geographically restricted. We used freshwater Gammarus to test this hypothesis. Sequences of two mitochondrial (cytochrome c oxidase subunit I and 16S) and two nuclear (28S and cytosolic heat-shock protein) genes were obtained for seven species distributed in 28 localities along the Lüliang and Taihang mountains in China. Phylogenetic analyses showed that Gammarus species were grouped into two clades, one from the Lüliang range and the other from the Taihang range. Each clade was further divided into three or four species, showing a congruent pattern with geographical vicariance. Divergence time estimation indicated that the split between the two clades coincided with the uplift of the Taihang Mountains at the boundary of Oligocene/ Miocene. Most speciation events may have been driven by massive uplifting of the Lüliang and Taihang mountains from the late Miocene to early Pliocene. Additionally, four new species are described: Gammarus incoercitus sp. nov., Gammarus benignus sp. nov., Gammarus monticellus sp. nov., and Gammarus pisinnus sp. nov. The new species are compared with related species in this area and a key to these species is provided. © 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 170, 591–633. doi: 10.1111/zoj.12119 ADDITIONAL KEYWORDS: HSP70 – mtDNA – speciation – taxonomy – time estimation. INTRODUCTION understanding of the historical processes that forge this correlation continues to develop. Several recent The correlation between phylogeny and geographical studies have demonstrated that geological events, distribution of aquatic organisms with poor dispersal such as mountain uplift, may play an important role ability is widely known (Seidel, Lang & Berg, 2009; in shaping the diversification patterns of animals Shih & Ng, 2011). Extensive planktonic dispersal (Renema et al., 2008; Weir & Price, 2011). is thought to promote gene flow and thus decrease The genus Gammarus Fabricius, 1775, is an ideal genetic differentiation. Therefore, organisms with model to investigate the relationship between the reduced dispersal should have strong structures diversification process and geographical distribution. over small spatial scales (Claramunt et al., 2012). Freshwater Gammarus are characterized by direct Numerous phylogeographical studies have found development of fertilized eggs in a marsupium and that well-supported clades are often distributed in no independent larval stage. Their weak dispersal rather well-defined geographical regions (Fišer, Sket potential means that they are easily influenced by & Trontelj, 2008; Hou et al., 2011). However, our geological barriers, such as mountain ranges, with their distributions often reflecting past geological *Corresponding author. E-mail: [email protected] events (Väinölä et al., 2008). In addition, species © 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 170, 591–633 591 592 Z. HOU ET AL. of Gammarus are particularly diversified in cool morphologically and genetically well-defined species running waters such as mountain streams, allowing according to the evolutionary species concept (Mayden, easy sampling for genetic studies. Moreover, most 1997), and we present formal taxonomic descriptions. species of Gammarus are highly endemic to a given landmass. For instance, the species group Gammarus pecos is narrowly endemic to the north-west Gulf MATERIAL AND METHODS of Mexico (Seidel et al., 2009) and the Gammarus SAMPLE COLLECTION fossarum group inhabits Europe (Westram et al., Samples of Gammarus were collected from 28 local- 2011), whereas several species are only found along ities along the Lüliang and Taihang mountain ranges the Lüliang and Taihang mountains in north China. (Fig. 1, Table 1). Freshwater Gammarus lacustris Gammarus shanxiensis Barnard & Dai, 1988 has Sars, 1863, Gammarus decorosus Meng, Hou & Li, been recorded in the southern region of the Taihang 2003, Gammarus komareki Schaferna, 1923, and Mountains (Mts), whereas Gammarus clarus Hou & saline Gammarus aequicauda (Martynov, 1931) were Li, 2010, is endemic to the northern part of the selected as outgroups based on previous phylogenetic Taihang Mts, and Gammarus nekkensis Uchida, 1935, analyses (Hou et al., 2011). exists largely to the far north of the Taihang range. Another four species were newly detected by the present authors during a detailed survey in 2012: DNA SEQUENCE AND PHYLOGENETIC ANALYSES Gammarus incoercitus sp. nov. and Gammarus Genomic DNA was extracted from the heads of speci- benignus sp. nov. were located in the northern and mens using a standard phenol chloroform isoamyl southern parts of the Lüliang Mts; Gammarus protocol (Hillis et al., 1996). Two mitochondrial gene monticellus sp. nov. and Gammarus pisinnus sp. nov. fragments of cytochrome c oxidase subunit I (COI) and were restricted to the south of the Taihang Mts. 16S rRNA with a small part of 12S rRNA, as well as These distinctive geographical patterns suggest that a nuclear gene coding for 28S rRNA were amplified uplifting of the Lüliang and Taihang ranges may have following published protocols (Hou, Fu & Li, 2007). promoted Gammarus speciation events. A fragment of the gene coding for cytosolic heat-shock The orogenic belt of the Taihang Mts runs in a protein (HSP70) was amplified using primers F498 north-to-south direction with an average elevation (5′-GACATGAARCAYTGGCCCTT-3′) and R960 (5′- of 1500–2000 m, dividing the Loess Plateau to the west CGCTTGAAYTCYTGGATGAAGT-3′) (Colson-Proch and the North China Plain to the east. At the early et al., 2010). PCR products were sequenced with the stage of the Miocene (23–16 Mya), the Taihang Mts BigDye terminator sequencing protocols on an ABI were rapidly uplifted to 800 m, followed by a stable 3730 DNA Analyzer. Automated sequence outputs period, then intensely elevated to approximately were imported into SEQUENCHER v. 4.5 (demo 1400 m at the Miocene/Pliocene boundary (6–5 Mya), edition, Gene Codes Corporation) for visual inspection reaching their current elevation at the end of the of the electropherograms. All sequences were aligned Pliocene (Gong, 2010). The Lüliang Mts rose rapidly using MAFFT v. 7.037 (Katoh & Standley, 2013) during the late Miocene (10–6.5 Mya), reaching an and adjusted by eye using MacClade v. 4.0 (Maddison elevation of 1500 m, finally resulting in the connection & Maddison, 2000). For COI and HSP70 sequences, of the Yellow River at 1.6 Mya (Li, 2009). The comple- we checked for the presence of pseudogenes using tion of the Taihang and Lüliang mountains formed the translated amino acid sequences based on Drosophila Shanxi rift between the two ranges. The complex mitochondrial or universal genetic code on MacClade. topography in this region presented a significant geo- The best-fit partitioning schemes and nucleotide graphical divider for the local fauna, and promoted substitution models were selected using Partition- many endemic species (Zhang, Xi & Li, 2006). Surpris- Finder v. 1.1.0 on the Bayesian information criterion ingly, very few investigations have been carried out to (Lanfear et al., 2012). The COI data were partitioned investigate the potential impact of such uplifts on into first, second, and third codon positions with equal- extant biodiversity. frequency Tamura-Nei (TrNef) plus Gamma distrib- In this study, we explored the morphology of uted rate variation among sites (G), transversion Gammarus specimens from the Lüliang and Taihang model (TVM) plus proportion of invariable sites (I), and ranges, and inferred a phylogeny based upon general time reversible with gamma distribution (GTR sequences of two mitochondrial genes and two nuclear + G) substitution models, respectively. The HSP70 genes to unravel the relationships between genetic gene was also partitioned for codon positions, with variation and geographical patterns. We also esti- Felsenstein 1981 (F81) for the first codon, Jukes- mated the divergence time to determine the diversifi- Cantor (JC) for the second codon, and GTR + G for the cation processes associated with the uplifts. In the third codon. The best-fit models for 28S and 16S were course of this study, we detected four undescribed GTR+I+G. © 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 170, 591–633 DIVERSIFICATION OF GAMMARUS SPECIES 593 Figure 1. Distribution map of Gammarus species along the Lüliang and the Taihang Mountains (Mts). Numbers and closed circles stand for species and their distributions. The red line represents the separation between the Lüliang Mts clade and the Taihang Mts clade. 1, Gammarus incoercitus sp. nov.;2,Gammarus benignus sp. nov.; 3, Gammarus shanxiensis;4,Gammarus monticellus sp. nov.;5,Gammarus pisinnus sp. nov.;6,Gammarus clarus; 7, Gammarus nekkensis. We inferred the phylogenetic relationships using constructing a majority consensus tree and estimat- maximum parsimony (MP), maximum likelihood
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