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Burlakova 1815 Final.Indd MALACOLOGIA, 2019, 62(2): 345–363 STATUS OF RARE ENDEMIC SPECIES: MOLECULAR PHYLOGENY, DISTRIBUTION AND CONSERVATION OF FRESHWATER MOLLUSCS TRUNCILLA MACRODON AND TRUNCILLA COGNATA IN TEXAS Lyubov E. Burlakova1*, David Campbell2 & Alexander Y. Karatayev1 ABSTRACT Freshwater bivalves in the family Unionidae are one of the most endangered groups of animals in North America. In Texas, where over 60% of unionids are rare or very rare, 15 species have been added to the state’s list of threatened species, and 10 are under con- sideration for federal listing. Due to insufficient survey efforts in the past decades, however, primary data on current distribution and habitat requirement for most of these rare species are lacking, thus challenging their protection and management. Although the species are listed as valid, there was no genetic confirmation to test for the possibility of ecophenotypes, which complicates conservation efforts. In this paper, we present genetic and distributional data for two rare Texas species, Truncilla macrodon and Truncilla cognata, and we suggest appropriate conservation measures. Tests of genetic affinities of these species using three gene regions, cox1, nad1 and ITS1, supported recognition of T. cognata and T. macrodon as full species. Analysis of historic and current species distribution showed that both these regional endemics are particularly vulnerable, and their distribution range has been reduced in the last 80 years. Key words: freshwater molluscs, Truncilla macrodon, Truncilla cognata, molecular identifica- tion, taxonomy, distribution, habitat requirements, conservation priorities. INTRODUCTION are very rare (Burlakova et al., 2011a). Due to its size, geological features and diverse Molluscs are among the most threatened landscapes, Texas is listed among the top animals on the planet: the number of mollusc U.S. states in species diversity and endemism extinctions worldwide is higher than the number (Stein, 2002), but the conservation status of of extinctions in all other taxa combined (Ré- most of Texas’ ecoregions is vulnerable or gnier et al., 2009). Among freshwater bivalves critical (Abell et al., 2000). The major threats world-wide, Unionida have the highest percent- to Texas freshwaters include damming, pollu- age of near-threatened, threatened and extinct tion, water extraction and urban development species (Lopes-Lima et al., 2018), similarly to (Dahm et al., 2005). As a result, the state of North America (Bogan, 1993; Lydeard et al., Texas ranks fourth in the country in terms of 2004) where over 76% of the Unionidae and the number of species extinctions (Stein, 2002). Margaritiferidae presumed extinct, threatened, Of the 15 unionid species listed as Texas state endangered or deemed of special concern threatened species (Texas Register 35, 2010), (Williams et al., 1993). Sensitivity to water ten are currently under consideration for fed- and habitat quality, long life span, sedentary eral listing by the U. S. Fish & Wildlife Service lifestyle, complex life cycle with parasitic larvae (Federal Register, 74, 66261, 2009; Federal requiring specific fish hosts, slow growth and Register, 74, 66866, 2009), and one species low reproductive rates are among the main (Popenaias popeii) has recently been added to reasons for their decline (reviewed in Bogan, the federal List of Endangered and Threatened 1993; Grabarkiewicz & Davis, 2008; McMahon Wildlife (Federal Register, 83, 5720, 2018). & Bogan, 2001; Strayer et al., 2004). Accurate identification is a necessary com- In the U. S. state of Texas, 65% of all unionid ponent for taxa monitoring and protection, but species are rare, and most endemic species few morphological characters are evident, 1Great Lakes Center, SUNY Buffalo State, 1300 Elmwood Ave., Buffalo, New York, 14222, U.S.A. 2Department of Natural Sciences, Box 7270, Gardner-Webb University, Boiling Springs, North Carolina, 28017, U.S.A. *Corresponding author: [email protected] 345 346 BURLAKOVA ET AL. making quantitative morphologically based In addition to limited distributional data, taxo- unionid taxonomy difficult (Roe & Hoeh, 2003) nomic status of both species is unclear as well. and resulting in many synonyms of morpho- Johnson (1999) combined T. cognata and T. logically variable taxa in the literature (e.g., macrodon with T. donaciformis, likely based on Burch, 1973; Ortmann, 1923; Simpson, 1914). a limited number of museum specimens and in Although our understanding of relationships absence of genetic analysis (Howells, 2010), within Unionidae has greatly increased over whereas other scientists recognize them as recent decades due to application of molecular separate species (Howells et al., 1996, 2010; tools, a limited number of phylogenetic studies Turgeon et al., 1998; Williams et al., 1993). In have been conducted on freshwater unionid this paper, we analyze genetic and distribu- mussels in Texas, and it is quite possible that tional data of T. macrodon, and T. cognata to some of the nominal species and genera do define their proper taxonomic status and bioge- not represent natural units. Conservational ography, and suggest conservation measures laws and methods cannot be implemented until to protect these rare endemic species. the endangered organism is properly clarified and its geographical range is known (Lydeard & Roe, 1998). The knowledge of genetic diver- MATERIAL AND METHODS sity is also important for captive breeding and reintroduction of endangered species, as it will Molecular Techniques be successful only if the genotypes used can tolerate particular conditions. Molecular investigation used three gene re- In this paper, we analyze genetic and distri- gions, cox1, nad1, and ITS1. DNA extraction butional data of two very rare Texas species: used Zymo DNA Tissue Miniprep kits. Primers Truncilla macrodon and T. cognata. Truncilla for cox1 were 5′-GTTCCACAAATCATAAGGA- macrodon was described by Lea (1859) from TATTGG-3′ and 5′-TACACCTCAGGGTGAC- Fayette County, Texas. The species is a very CAAAAAACCA-3′, adapted from Folmer rare central Texas endemic (Howells et al., et al. (1994). Primers for nad1 were 5′-TG- 1996, 1997) and is currently under consid- GCAGAAAAGTGCATCAGATTTAAGC-3′ and eration for federal listing by the U. S. Fish & 5′-GCTATTAGTAGGTCGTATCG-3′ (Buhay et Wildlife Service (Federal Register, 74, 66261, al., 2002; Serb & Lydeard, 2003), and primers 2009). Although reported by Strecker (1931) for ITS1 were 5′-AAAAAGCTTCCGTAGGT- as “an abundant shell in the Colorado and GAACCTGCG-3′ and 5′-AGCTTGCTGCGT- Brazos rivers”, less than 200 specimens of T. TCTTCATCG-3′ (King et al., 1999). The primer macrodon had been reported until recently, and LoGlyR (5’-CCTGCTTGGAAGGCAAGTG- even fewer were alive at the time of collection TACT-3’) (Serb et al., 2003) was used as an (Howells, 2010, 2011). Due to their rarity, T. additional external primer option for nad1 macrodon biology and ecology, including repro- and primers UNIOCOII.2 (5’-CAGTGGTAT- ductive cycle, potential fish hosts and habitat TGGAGGTATGAGTA-3’) from Walker et al. have never been studied (Howells, 2010). (2007) and/or HCOout (CCAGGTAAAAT- Truncilla cognata is endemic to the Rio Grande TAAAATATAAACTTC; Carpenter & Wheeler, drainage (Neck, 1984) and was described 1997) were used as external primers for some from Rio Salado, Mexico (Lea, 1857). Taylor cox1 amplifications. PCR used 10 min denatur- (1966) believed that T. cognata is “one of the ing at 95°C, followed by 40 cycles of 95°C for few mussels … that is actually endangered”. 30 sec, 5°C under the annealing temperature This species is considered endangered by the of the lower-annealing primer for 30 sec, and American Fisheries Society (Williams et al., 60 sec at 72°C, and then a final 10 min hold at 1993), listed as threatened in Texas (Texas 72°C. PCR products were cleaned with Zymo Register 35, 2010), and is under consideration DNA Clean & Concentrator kits and sequenced for federal listing by the U. S. Fish & Wildlife by Macrogen. For all phylogenetic analyses, Service (Federal Register, 74, 66261, 2009). identical sequences were combined into a During the last 100 years, T. cognata was re- single sequence. Sequences were aligned in ported only from a few sites in the Rio Grande BioEdit (Hall, 1999) and, for the ITS region, drainage in Texas (Karatayev et al., 2012). This with MAFFT (Katoh & Standley, 2013), followed species is likely to be present in Mexico, but by manual editing to check for consistency in no data exist from the Mexican portions of the the alignment. The data were analyzed using Rio Grande, limiting the estimation of species’ PAUP* 4.0 a159 (Swofford, 2002), TNT 1.5 geographic range and conservation status. (Goloboff & Catalano, 2016), MrBayes 3.2 ENDEMIC TRUNCILLA SPP. IN TEXAS 347 (Ronquist et al., 2012), and bppX (Xu, 2012, was used to reveal the presence of mussels a user interface for the BP&P 3.1 program of and species diversity (Strayer et al., 1997; Yang, 2015). Gaps were coded as missing Vaughn et al., 1997) at all sites (Karatayev et data. The sequences were concatenated, and al., 2012, 2018a). Due to poor water visibility, identical sequences were grouped together tactile searches (running fingers over the sedi- for parsimony and Bayesian analyses. Maxi- ment, usually up to 15 cm deep, depending on mum parsimony analyses used 500 random substrate type) were used at all sites. Collected replicates. Jackknife analyses used 500 repli- live mussels and shells were counted and cates, each using a random parsimony search measured with calipers to the nearest mm, and of 10 replicates. We used the GC jackknife then live mussels were carefully bedded back value, which subtracts support for competing into the sediment from which they were taken. clades as a more conservative evaluation of Shell condition of dead mussels was recorded the support level (Goloboff et al., 2003). Both for each shell. When surveys were conducted used all of the “new technology” tree search from private land, landowner permission was options in TNT. Automated model selection in acquired from each property owner before PAUP* favored a TVM+I+G model, which was entering the property.
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