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Identity of Freshwater Shrimp Populations (Palaemon Weber, 1795) from Northern Mexico: Genetic Variation at Local and Regional Scales

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Identity of Freshwater Shrimp Populations (Palaemon Weber, 1795) from Northern Mexico: Genetic Variation at Local and Regional Scales JOURNAL OF CRUSTACEAN BIOLOGY, 34(4), 481-493, 2014 IDENTITY OF FRESHWATER SHRIMP POPULATIONS (PALAEMON WEBER, 1795) FROM NORTHERN MEXICO: GENETIC VARIATION AT LOCAL AND REGIONAL SCALES Fernando Álvarez 1, Carlos Pedraza-Lara 1,2,∗, and José Luis Villalobos 1 1 Colección Nacional de Crustáceos, Instituto de Biología, Universidad Nacional Autónoma de México, Apartado Postal 70-153, México 04510, D.F., México 2 Colección Nacional de Insectos, Instituto de Biología, Universidad Nacional Autónoma de México, Apartado Postal 70-153, México 04510, D.F., México ABSTRACT The freshwater genus Palaemon is widely distributed in north-eastern Mexico, where six species have been recognized. Of special interest is the area of the Cuatro Cienegas Valley (CCV) and the Salado and Bravo Rivers basins in central and northern Coahuila, where interconnections, ancient and contemporary, have created a mosaic of populations of species belonging to Palaemon that cannot unequivocally be assigned to one species. We seek to encompass the species determination in a phylogenetic framework by reconstructing phylogenetic relationships of the aforementioned populations and 4 of the species occurring in México. We collected information of three genetic fragments (COI, 12S, and H3) and performed maximum likelihood and Bayesian inference phylogenetic analyses. Also, through the analysis of a partial sequence of the cytochrome oxidase subunit I gene (COI) from individuals coming from 22 populations, we explored phylogeographic patterns from the three basins. Relaxed molecular clock were carried out focused on dating the cladogenesis of all species, while mismatch and Bayesian Skyline Plots analyses were used to test for possible demographic changes in populations from CCV. Gene-separated and concatenated phylogenetic analyses supported the monophyly of the species described from Mexico, but did not show their inclusion in one monophyletic clade, rather depicting a structure congruent with multiple invasions to freshwater. Dating analysis provided long-term temporal framework for cladogenesis. Three different lineages were found in the CCV, confirming the high diversity of this region. One of them is identified with P. sutkussi, and two are possible new species to science. Haplotype analyses provided insight from recent population processes and are congruent with a scenario where despite keeping signatures of past cladogenesis, more recent genetic structure reveals surprisingly higher connectivity between basins associated to the Bravo river system and CCV. KEY WORDS: distribution, drought, freshwater shrimp, genetics, protected areas, systematics DOI: 10.1163/1937240X-00002248 INTRODUCTION paludosus (Gibbes, 1850) (Baja California), and P. suttkusi Palaemon has a cosmopolitan distribution and after its (Strenth, 1976) (Coahuila). The identity of each of these taxonomic re-appraisal, includes 83 marine, estuarine and species in Mexico seemed to be a resolved matter until re- freshwater species (De Grave and Ashelby, 2013). The cently, when more intensive sampling was conducted in the taxonomy of the genus is complex because of the reduced Cuatro Ciénegas Valley (CCV) and the neighboring Sabinas number of useful characters to discriminate among species, River basin, northern Coahuila. Captured shrimp from these and because these characters have a limited extent of trips showed differing morphology to that of P. suttkusi, variation. The dentition of the rostrum and the spinulation which is the species described for the region and could not of the appendix masculina, both with a small range of be assigned to this species unequivocally. In a recent paper variation, are the main examples of taxonomically important on the phylogeography of P. suttkusi from the CCV, Chaves- characters for this genus and related palaemonids (Ashelby Campos et al. (2011) explored the relationship between the et al., 2012). Typically, small morphological variations populations of P. suttkusi from the CCV and the Río Sal- associated to disjunct or isolated distributions, have been ado, which is a neighbouring basin to the CCV. They iden- used to describe and differentiate species (Ashelby et al., tified two different lineages based on 27 COI haplotypes; 2012; De Grave and Ashelby, 2013). however, they could not decide whether the observed vari- In regards to habitat type, six freshwater species of Palae- ation could support the description of a second species for mon (formerly included in the junior synonym Palaemon- the region. The two lineages were identified both inside and etes) occur in northern Mexico: P. hobbsi (Strenth, 1994) outside the CCV making it difficult to provide an accurate (Tamaulipas), P. kadiakensis (Rathbun, 1902) (Coahuila), P. taxonomic framework in which define proper conservation lindsayi (Villalobos-Figueroa and Hobbs, 1974) (San Luis measures of these shrimps in the CCV. Evidence emerging Potosi), P. mexicanus (Strenth, 1976) (San Luis Potosi), P. from the aforementioned issues with species discrimination ∗ Corresponding author; e-mail: [email protected] © The Crustacean Society, 2014. Published by Brill NV, Leiden DOI:10.1163/1937240X-00002248 482 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 4, 2014 using morphology data, together with the genetic variabil- sequences were deposited in GenBank and alignments are available from ity detected, made it plausible to suspect on the presence of the authors upon request. cryptic diversity in several populations from the CCV. Our Phylogeny: COI Genealogy and Concatenated Analyses work here attempts to attain taxonomic certainty concern- After trimming of possible primer sites was done, all data sets were ing these populations, which is of primary importance for aligned using MUSCLE (Edgar, 2004). For COI data, recommendations conservation within the protected areas scheme in Mexico to detect the occurrence of nmtDNA were carried out for each sequence, (Cabral and Cruz, 2007). which included the identification of stop codons and a high frequency of non-synonymous substitutions as well as unusual levels of genetic Our study examines the genetic identity of the populations divergence in samples coming from one population (Song et al., 2008; of Palaemon from the CCV in order to answer the following Buhay, 2009). As outlined before, we carried out an initial evaluation of questions: 1) do the populations of CCV belong to one or phylogenetic structure using data from COI only. From the data set I (153 several species? 2) what is the current distribution of P. individuals, 601 bp), mitochondrial COI sequences were collapsed into suttkusi unique haplotypes using DnaSP v. 5 (Librado and Rozas, 2009), and a ? 3) do the CCV and the basin of the Sabinas River phylogenetic inference was carried out with this haplotype data, which function as separate systems or is it a common basin? and we term data set II (62 individuals and 601 bp). Subsequently, a second 4) what is the degree of divergence among populations when phylogenetic analysis was carried out with representatives from COI mt- the comparison includes three other species, P. kadiakensis, lineages only, conforming a concatenated matrix together with 12S and P. lindsayi and P. mexicanus? H3 fragments, which we term data set III (14 individuals and 1298 bp, see Table 1). Phylogenetic procedures here described were applied to data set II and III. In order to identify the most appropriate evolutionary MATERIALS AND METHODS model by the Akaike corrected information criterion (AICc), the program jModeltest v. 0.1.1 (Posada, 2008) was used. Phylogenetic analyses were Acquisition of Samples conducted using maximum likelihood (Ml) with the computer program A total of 153 COI-sequences, which included 53 newly generated PhyML (Guindon and Gascuel, 2003). We assessed confidence in branches sequences, and accounted for four of the five species naturally occurring using 1000 nonparametric bootstrap replicates under the most accurate in Mexico, were processed for the present analysis (Table 1, Fig. 1). Our evolutionary model. This model was also used to carry out Bayesian sampling was conducted between 2010 and 2012 in six trips to the CCV and inference (BI) of phylogeny as implemented in MrBayes v. 3.1.2 (Ronquist the Sabinas River basin. Palaemon mexicanus and P. lindsayi were collected and Huelsenbeck, 2003), applying a Monte Carlo Markov Chain (MCMC) in their type localities: Santa Anita stream near Ciudad Valles and Media procedure after 5 million generations, and partitioned by codon position for Luna Lagoon, both in San Luis Potosi, respectively. Palaemon kadiakensis data set I and additionally by gene for data set II. Convergence between was collected in several localities along the Bravo River from La Amistad the different parameters in paired simultaneous analyses (4 chains by run) and run length were adjusted considering an adequate sampling based on Dam to Piedras Negras, Coahuila. Seeking to cover most of the genetic average standard deviation of split frequencies being <0.01 (Huelsenbeck variation, the analysis also considered 100 COI identified as P. suttkusi in and Ronquist, 2005). The burn-in period was determined as the set of trees GenBank from a previous study (Chaves-Campos et al., 2011a), which were saved prior to log likelihood stabilization and convergence as estimated especially useful to describe patterns of variability inside the CCV. In total, using Tracer 1.4 (Rambaut and Drummond, 2007). Tracer v. 1.4.1 was used 22 populations assigned to different species of
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