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Evidence of Stream Capture from the Tallapoosa River Drainage by a Chattahoochee River Tributary Based on Fish Distributions
Andrew Jarrett, Warren Stiles, Alexis Janosik, Rebecca Blanton, and Carol Johnston

Southeastern Naturalist, Volume 16, Issue 1 (2017): 117–136

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Southeastern Naturalist 117 A. Jarrett, W. Stiles, A. Janosik, R. Johansen, and C. Johnston 22001177 SOUTHEASTERN NATURALIST 1V6o(1l.) :1161,7 N–1o2. 61 Evidence of Stream Capture from the Tallapoosa River Drainage by a Chattahoochee River Tributary Based on Fish Distributions Andrew Jarrett1, Warren Stiles1, Alexis Janosik2, Rebecca Blanton3, and Carol Johnston1,* Abstract - Based on the distribution of 2 fish species and geological ev idence, we propose stream capture of a Tallapoosa River tributary by Wehadkee Creek, a tributary of the Chattahoochee River in east-central Alabama. Micropterus tallapoosae (Tallapoosa Bass) and Cyprinella gibbsi (Tallapoosa Shiner), endemics to the Tallapoosa River drainage, are found in Wehadkee Creek (Chattahoochee River drainage). We used mitochrondrial DNA to compare the Wehadkee Creek specimens of Tallapoosa Shiner to those analyzed in a previous study of the genetic structure of the species throughout the Tallapoosa River drainage. Their identity as Tallapoosa Shiner was validated, and we found some divergence relative to other populations in the Wehadkee Creek fish. We validated the identity of Tallapoosa Bass and Micropterus chattahoochae (Chattahoochee Bass), using mitochondrial DNA sequences subjected to phylogenetic analyses of all Micropterus coosae (Redeye Bass) group species previously identified. In addition to these fish distributions, the geology of the upper Wehadkee Creek area suggests a past stream capture may have occurred. Alternatively, these fishes could have been introduced into adjoining drainages by hu mans. Introduction Distributions of freshwater organisms can offer clues to past drainage configuration (Mayden 1988). In some cases, a species with a broad distribution in one drainage can be found in a small portion of an adjacent drainage. If the pattern of distribution is repeated in other species, a case can be made for a chance event, such as stream capture, playing a role in the distribution of these species (Wiley 1988). The process of streams being displaced from one drainage to another is termed river capture (Bishop 1995). The distribution and relationships among fishes have been used to infer stream capture and drainage modification in several river systems. One of the most obvious indications of geologic drainage modification based on distribution of fishes are the 11 species of Mobile Basin endemic fishes found in Bear Creek, Alabama and Mississippi, which currently flows into the Tennessee River (Wall 1968). These fishes are found nowhere else in the Tennessee River drainage, strongly suggesting stream capture of a Mobile Basin stream by a Tennessee River tributary. However, not all distributional 1Fish Biodiversity Lab, School of Fisheries, Aquaculture and Aquatic Sciences, Auburn University, Auburn, AL 36849. 2University of West Florida, Department of Biology, Building 58/60, 11000 University Parkway, Pensacola, FL 32514. 3Department of Biology, Austin Peay State University, PO Box 4718, 681 Summer Street, Clarksville, TN 37040. *Corresponding author - Manuscript Editor: Benjamin Keck Southeastern Naturalist A. Jarrett, W. Stiles, A. Janosik, R. Johansen, and C. Johnston 2017 Vol. 16, No. 1 118 evidence of drainage modification is as striking, and other lines of evidence are brought to bear. Most modern studies testing hypotheses regarding past river capture use genetic analysis of fishes or other aquatic organisms to investigate phylogeographic relationships within a single species (Howard and Morgan 1993, Hurwood and Hughes 1998, Waters et al. 2001). Waters et al. (2001) used mitochondrial DNA sequence data to examine a geomorphic hypothesis used to explain the distribution of a species complex of freshwater Galaxias. The data suggested that an isolated population otherwise restricted to Clutha/Kawarau River system found in the Nevis River diverged at approximately the same time as a water-flow reversal, resulting in headwater capture. Some studies have used genetic relationships within multiple species to test hypotheses regarding river capture (Burridge et al. 2006). Using mitochondrial DNA of 2 galaxiids, Burridge et al. (2006) provided evidence of stream capture. Divergence between 2 sister species was low in streams thought to have undergone stream capture, while in other areas divergence between study species was high. Typically the scale of these studies includes several streams or river reaches, although some focus on a single stream (Wall 1968). Combining evidence from the distribution and evolutionary relationships of fishes has enabled the inference of several river-modification events throughout the world. We hypothesize that the distribution of 2 fish species in east-central Alabama may be the result of past stream capture. We documented 2 species (Micropterus tallapoosae Baker, Johnston, and Blanton [Tallapoosa Bass] and Cyprinella gibbsi (Howell and Williams) [Tallapoosa Shiner]) endemic to the Tallapoosa River drainage in a single stream, Wehadkee Creek, of the Chattahoochee River drainage, Alabama. The presence of Tallapoosa Shiner in Wehadkee Creek was previously documented, but thought to be a bait-bucket introduction (Boschung and Mayden 2004). During a survey for Micropterus chattahoochae Baker, Johnston, and Blanton (Chattahoochee Bass), a Chattahoochee River endemic, in Wehadkee Creek, we documented the occurrence of Tallapoosa Bass. Given that there are 2 species involved, we propose that a headwater stream capture may have occurred between Wehadkee Creek (Chattahoochee River drainage) and a tributary of the Tallapoosa River drainage. The alternative explanation is that these species were separately introduced into streams where they were not indigenous. We present data on the distribution of Tallapoosa Bass, Chattahoochee Bass, and Tallapoosa Shiner in Wehadkee Creek, AL. Genetic analyses are also presented to confirm the identity of focal species and examine phylogeographic structure. Field-Site Description Wehadkee Creek (Fig. 1) was chosen as a survey site for Chattahoochee Bass to fill knowledge gaps regarding its distribution in Alabama, where it was not known to occur. Prior surveys for basses in other major Chattahoochee River tributaries did not detect species of the Micropterus coosae Hubbs and Bailey (Redeye Bass) species group (Macenia et al. 2007). A search for museum records of species from this group revealed 2 records: 1 specimen collected in 2001 and 1 from a 1972 Southeastern Naturalist 119 A. Jarrett, W. Stiles, A. Janosik, R. Johansen, and C. Johnston 2017 Vol. 16, No. 1 collection. Both were identified as Micropterus coosae because M. tallapoosae and M. chattahoochee were not recognized at the time. This 3rd-order stream originates as a spring just north of High Shoals, and flows through piedmont upland Figure 1. Sampling sites in the High Pine and Wehadkee watersheds. Southeastern Naturalist A. Jarrett, W. Stiles, A. Janosik, R. Johansen, and C. Johnston 2017 Vol. 16, No. 1 120 physiography before entering West Point Reservoir on the Chattahoochee River in east-central Alabama (Fig. 1). The size and upland physiography of Wehadkee Creek were assumed to be suitable habitat for Chattahoochee Bass, but a recent survey of stream fishes was lacking. High Pine Creek (Tallapoosa River drainage) was sampled for Tallapoosa Shiner to provide material for comparison to Tallapoosa Shiner from Wehadkee Creek. Samples from this stream were not included in the analysis by Connelly et al. (2006). Our sample sites in this upland stream were taken from 2nd-order sites in close proximity to Wehadkee Creek. Methods We sampled 9 sites in Wehadkee Creek (Chattahoochee River drainage) for Chattahoochee Bass (Fig. 1, Table 1). In addition, we sampled a nearby tributary of the Tallapoosa River, High Pine Creek (HP1, HP2), for Tallapoosa Shiner for genetic analysis (n = 2 sites). Basses were collected using a backpack electrofisher, anesthetized using MS 222, photographed, and measured (standard length, SL, mm). We used seines to collect Tallapoosa shiners. Prior to anesthetizing and releasing all target species captured, we biopsied fins and placed the samples in 95% ethanol for genetic analysis. Specimens were vouchered at the Fish Biodiversity Lab. Treatment and handling methods were approved by Auburn University animal protocol #2012-2166. Using the DNeasy Blood and Tissue Kit (Qiagen, Inc.) and following the manufacturer’s directions, we extracted genomic DNA from fins of 4 specimens of Tallapoosa Bass and 2 specimens of Chattahoochee Bass from Wehadkee Creek. Resulting DNA was sequenced for the mitochondrial NADH subunit 2 gene (ND2) and compared to individuals sequenced for a prior study of Redeye Bass systematics (Baker et al. 2013) to validate species identifications. Methods of PCR amplification and sequencing followed those of Baker et al. (2013). We obtained comparative sequences, including outrgroup taxa (Micropterus salmoides (Lacepède) [Largemouth Bass]) generated by Baker et al. (2013), from GenBank. Table 1. Collection sites. Site numbers correspond to those in F igure 1. Site Description County State Latitude Longitude Date W1 Wehadkee Creek at Rock Mills Randolph AL 33.15744 -85.28846 06/08/15 W2 Little Wehadkee Creek at CR 20 Heard GA 33.15056 -85.24068 06/16/15 W3 Wehadkee Creek at CR 30 Randolph AL 33.19784 -85.27825 06/16/15 W4 Wehadkee Creek at CR 638 Randolph AL 33.22586 -85.32030 06/10/15 W5 High Shoals Falls (below) Randolph AL 33.23682 -85.33214 07/06/15 W6 High Shoals Falls (above) Randolph AL 33.23783 -85.33383 07/06/15 W7 Unnamed tributary at CR 645 Randolph AL 33.25327 -85.33121 06/16/15 W8 Wehadkee Creek at CR 634 Randolph AL 33.25343 -85.32271 06/10/15 W9 Wehadkee Creek at CR 633 Randolph AL 33.26336 -85.30775 06/16/15 HP1 High Pine Creek at CR 16 Randolph AL 33.20264 -85.34325 06/10/15 HP2 High Pine Creek at CR 59 Randolph AL 33.23132 -85.35699 07/06/15 Southeastern Naturalist 121 A. Jarrett, W. Stiles, A. Janosik, R. Johansen, and C. Johnston 2017 Vol. 16, No. 1 We used data from 38 Wehadkee Creek and High Pine Creek Tallapoosa Shiner, along with data from Connelly et al. (2006), in a genetic analysis. Specimens from these streams were not included in their study. Again using the DNeasy Blood and Tissue Kit and following the manufacturer’s directions, we extracted genomic DNA. The mitochondrial NADH 4L dehydrogenase (ND4L) gene of 312-bp was amplified using polymerase chain reaction (PCR). We sequenced amplified products bi-directionally with GenWiz, Inc. (New Brunwick, NJ). We downloaded from Genbank ( sequences (Haplotypes A-L) from Connelly at al. (2006) of ND4L to include in the analysis, and used Cyprinella trichroistia (Jordan and Gilbert) (Tricolor Shiner) as an outgroup. See Connelly et al (2006) for details on PCR and sequencing methodology . We examined the phylogenetic and phylogeographic structure within the Tallapoosa Shiner and Redeye Bass species group using Bayesian analyses. Prior to the Bayesian analysis, we deteremined the optimal model of sequence evolution for each data set (ND4L and ND2, respectively) by evaluation of likelihood scores for 56 progressively complex models using MrModeltest v2 (Nylander 2004). The best-fit model and its parameters (GTR+G for both) selected under the Akaike Information Criterion (AIC) were implemented in MrBayes 3.1.1 (Ronquist and Huelsenbeck 2003). We used 4 Markov chains with flat priors in all analyses and started each chain with random trees. Runs consisted of 10 million generations of Markov chain Monte Carlo (MCMC) simulations. We conducted 2 replicate runs to ensure the MCMC went through a sufficient number of iterations to allow convergence in the estimations of tree topology with the best maximum likelihood posterior probability. The burn-in of the MCMC analysis was determined by graphically examining the ML scores at each of the sampled generations to find where values converged. We discarded all trees recorded prior to the burn-in and used the remaining trees to compute a majority rule consensus tree. Posterior probabilities (pp) were used as an indication of node support. Results We collected Tallapoosa Bass (n = 10) at 6 sites in Wehadkee Creek, and found Chattahoochee Bass (n = 2) at 1 site (Fig. 1, Table 1). We genetically analyzed 6 specimens. Tallapoosa Bass were found at our uppermost sample sites (W4 and W8), while Chattahoochee Bass were found downstream at site W1. Tallapoosa Shiners were found at most sites downstream of High Shoals Fall s (Fig. 1). Relationships among redeye basses are discussed in detail in Baker et al. (2013). The analysis conducted herein recovered the same relationships as observed in that previous study and confirmed species identifications based on examination of morphological traits typical of the 2 species collected in Wehadkee Creek, Tallapoosa Bass and Chattahoochee Bass (Fig. 2). Tallapoosa Bass specimens had green caudal fins, soft dorsal and anal fins, 11 lateral blotches, and no tooth patch. Chattahoochee Bass had orange tips on caudal fins, soft dorsal and anal fins, 9 lateral blotches, and tooth patches of 2.0 mm and 24 mm. All individuals identified Southeastern Naturalist A. Jarrett, W. Stiles, A. Janosik, R. Johansen, and C. Johnston 2017 Vol. 16, No. 1 122 by these morphological traits as either Tallapoosa Bass or Chattahoochee Bass from Wehadkee Creek were recovered in their respective species clades stemming from analyses of the mitochondrial ND2 gene (Fig. 2). Although some divergence is evident from Tallapoosa Shiner specimens found at Wedhadkee Creek and High Pine Creek, the majority of individuals are closely related to other populations of Tallapoosa Shiner from Connelly et al. 2006 (Fig. 3). Moreover, genetic divergence is low between most individuals from Wedhadkee Creek, High Pine Creek, and the Tallapoosa River locations, resulting in low levels of geographic structure in the gene tree. We included data from High Pine Creek, which is in very close proximity to Wehadkee Creek (Fig. 1) to see if there was a genetic signature uniting these 2 populations, which might suggest an origin of the Tallapoosa Shiner population in Wehadkee Creek. However, we did not see a closer relationship between these 2 populations and other sources of Tallapoosa Shiner. Figure 2. Majority rule consensus resulting from the post-burnin Bayesian analysis of the ND2 gene for members of the Redeye Bass species group. Letters following species names correspond to those in Table 1 of Baker et al. (2013). Those generated herein, from Wehadkee Creek labeled using site numbers (W1, W4, and W8) in bold that correspond to site information in Table 1 and Figure 1. Asterisks indicate well-supported nodes with posterior probabilities of 0.98 or higher. Outgroup taxa not shown. Southeastern Naturalist 123 A. Jarrett, W. Stiles, A. Janosik, R. Johansen, and C. Johnston 2017 Vol. 16, No. 1 Discussion The distribution of Tallapoosa Bass and Tallapoosa Shiner in Wehadkee Creek (Chattahoochee River drainage) suggests a potential stream-capture event involving the Tallapoosa and Chattahoochee drainages in east-central Alabama, as these species are otherwise found only in the Tallapoosa River drainage. Although one of these species is a minnow, and could be the result of a bait-bucket transfer, the other is a species of non-game bass, a less likely candidate for human introduction. The occurrence of 2 species in drainages outside their much larger ranges can be considered a repeated pattern, evidence for a chance event (Wiley 1988). Wall (1968) provided both geologic and distribution data for 11 taxa of fishes that supported Figure 3. Bayesian inference topology for ND4L sequence data of Tallapoosa Shiner. Number next to node indicates posterior probabilities. Site numbers correspond to those in Table 1 and Figure 1. Southeastern Naturalist A. Jarrett, W. Stiles, A. Janosik, R. Johansen, and C. Johnston 2017 Vol. 16, No. 1 124 headwater capture of the Bear Creek system by the Tennessee River. Similarly, Jenkins et al. (1972) documented the transfer of 6 species from the Casselman River drainage to the Potomac River via distributional and geologic evidence. Other studies of possible stream captures have examined the genetic relationships of single species to trace potential transfers by looking at patterns of genetic similarity and divergence (Howard and Morgan 1993, Strange 1998). We used genetic analysis to verify the identity of Tallapoosa Shiner and Tallapoosa Bass, and to examine potential patterns of genetic relatedness within Tallapoosa Shiner (where there was sufficient sample size). Although we found some divergence among individuals of Tallapoosa Shiner from the Wehadkee Creek system, it is uninformative in regards to the drainage relationships. The distribution of a third species might also be explained by the same streamcapture event. Luxilus zonistius Jordan (Bandfin Shiner) is widely distributed throughout the Chattahoochee River drainage and is also found in a much smaller number of streams in the upper Tallapoosa River drainage (Boschung and Mayden 2004). Boschung and Mayden (2004) proposed introduction by humans as an explanation for the occurrence of Bandfin Shiner in Tallapoosa River streams. However, we suggest that given the location of Bandfin Shiner populations in relation to Wehadkee Creek (very close proximity), this species may have gained access to the Tallapoosa River drainage via the same capture event or similar repeated capture events that may have transferred Tallapoosa Bass and Tallapoosa Shiner into the Chattahoochee River drainage. Further evidence of a potential stream-capture event comes from the geological record. Upper Wehadkee Creek (Chattahoochee River drainage) lies along the Brevard fault zone, which runs through Randolph and Chambers counties in Alabama (Medlin and Crawford 1973). The current configuration of Wehadkee Creek as it crosses the fault suggests stream offset, and perhaps capture, of a nearby Tallapoosa tributary, via an earthquake or strike slip (Wallace 1968). Many stream channels show a characteristic sharp jog to the left in these areas, and are high gradient, which is true of the upper Wehadkee Creek system (Fig. 1; Schulz and Wallace 2013, Wallace 1968). In addition, evidence of the garnet-mica schist found in sections of the Brevard Fault can be found in abundance at High Shoals, providing evidence that the underlying topography is part of the fault. The timing of these geologic events is unknown. Fish distributions are often difficult to explain in light of human modifications. However, with 3 species suggesting entries into reciprocal drainages in 1 area, together with geological evidence that suggests conditions were conducive to stream capture, we believe that such an event was responsible for moving 2 Tallapoosa River endemics into Wehadkee Creek (Chattahoochee River drainage) and a Chattahoochee River endemic into the Tallapoosa River drainage. Additional work to estimate timing of the possible transfer, relative to clade divergence times, would provide a more robust explanation of the possible historical event or events that have contributed to the observed repeated crossdrainage distributions of our focal species. Southeastern Naturalist 125 A. Jarrett, W. Stiles, A. Janosik, R. Johansen, and C. Johnston 2017 Vol. 16, No. 1 Acknowledgments We thank Steve Rider, Meagan Roy, and Maria Jarrett for help with field work. We are grateful to the Belcher family for access to High Shoals, and to Erin Bloom and Mattie Lewis for assistance with lab analysis. 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