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Genetic Assessment of Reinforcement of the Japanese Brown Frog（Rana Japonica）

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Genetic Assessment of Reinforcement of the Japanese Brown Frog（Rana Japonica） Full paper Animal genetics Genetic Assessment of Reinforcement of the Japanese Brown Frog（Rana japonica） Mitsuaki OGATA1 ）＊ and Hiroshi SICHIRI2） 1）Preservation and Research center, City of Yokohama, Kanagawa, 241-0804, Japan 2）Yokohama Environmental Science Research Institution, Kanagawa, 221-0024, Japan ［Received 1 March 2018; accepted 7 January 2019］ ABSTRACT To assess the genetic suitability of reinforcement of two populations of the Japanese brown frog (Rana japonica) in Yokohama City, we attempted to clarify their genetic relationship based on sequence variation of mitochondrial DNA control region and polymorphism of 10 microsatellite DNA loci. The results showed that these two populations are genetically related, though they are presently isolated. This appears to conform to the conditions for reinforcement of the two populations. Key words: genetic variation, habitat fragmentation, reinforcement － Jpn J Zoo Wildl Med 24（1）：1-7, 2019 second most populous city and is highly urbanized [12]. Despite INTRODUCTION this high urbanization, Yokohama City is the main habitat of The worldwide decline of amphibian populations has been the frog in Kanagawa Prefecture [13]. However, in Yokohama previously reported [1]. Several factors have been proposed City, marshes, rice fields and other green spaces have as the cause of the decline, such as pollution, habitat loss, drastically reduced over the past 40 years (46.4% of the total ultraviolet radiation, and pathogens (e.g. [1]). Of these, habitat area in 1975 compared with 28.8% in 2015) [14], reducing loss and fragmentation are major factors [2], as they reduce the frog’ s available habitat. We predict a concurrent reduction population size, and lead to detrimental genetic effects such in the population. Indeed, the number of spawned egg masses as genetic load, inbreeding depression and reduced genetic reduced drastically during the last decade in the northern variation (e.g. [3-5]). To prevent such detrimental effect in small population in Yokohama City (P5 in Table 1). According to a populations, reinforcement (also known as augmentation), previous study, 757 egg masses were spawned in 2001 [13], defined as introduction of new individuals into a population of but in 2015, this number was estimated to be less than 50 conspecifics, is effective for supplying a new genetic resource [15]. Such drastic reduction led us to predict extinction of the [6-7]. Several translocations of amphibian species have already local population would occur unless conservation efforts were been reported [8]. applied to the population. Another large R. japonica population The Japanese brown frog, Rana japonica, is endemic to the was known to exist nearby (P6 in Table 1), although the two Japanese archipelago. This frog lives in hillside areas and populations are isolated by residential areas [13, 15]. In fact, spawns egg masses in water in marshes or rice fields during the these two populations are the largest (P6) and second largest early spring [9-10]. This frog has been assigned a vulnerable (P5) R. japonica populations in Kanagawa Prefecture [13]. status in several areas, including Kanagawa Prefecture [11]. Therefore, local extinction of P5 would greatly negatively Yokohama City, located in Kanagawa Prefecture, is Japan’s impact overall R. japonica levels in the prefecture. To prevent local extinction of P5, reinforcement from P6 was expected to be an effective approach. The genetic relationship between the * Corresponding author：Mitsuaki OGATA source population and the recipient population is important （E-mail: [email protected]） － 1 － Mitsuaki OGATA et al. Table 1 Locations and haplotypes in control region of mitochondrial DNA. Population No. of frogs Sample Location Haplotype P1 4 egg 35.566583, 139.495604 CR1(3/4),CR5(1/4) P2 2 tadpole 35.55615, 139.584683 CR6 (2/2) P3 4 egg 35.548467,139.568515 CR5 (4/4) P4 3 tadpole 35.539967, 139.579324 CR6 (3/3) P5 14 egg, finger 35.51336, 139.51572 CR2 (14/14) P6 11 egg, finger 35.503494, 139.534341 CR3 (7/11),CR4 (4/11) P7 2 tadpole 35.40828, 139.52122 CR7 (2/2) Total 40 Numbers in parentheses indicate the ratio corresponding to each haplotype. factor in the effectiveness of reinforcement, so as to prevent using ABI 310 genetic analyzer (Applied BioSystems) according outbreeding depression and encourage genetic rescue (e.g. [7, to the manufacturer’s instruction. DNA alignment was 16]). However, no information on the genetic relationship of performed with MEGA6 [18]. For estimating DNA divergence, the two populations has been reported so far and there is no we excluded sites where gaps or insertions were observed. information on the genetic relationships among the various R. Nucleotide diversity and haplotype diversity of two populations japonica populations in Yokohama City, which is necessary for (P5 and P6) was estimated using DnaSP ver. 5.1 [19]. The assessing the genetic suitability of reinforcement from P6 to effective number of migrants per generation (Nm) and fixation P5. Therefore, in this study, we investigated genetic relationships among the populations of R. japonica in Yokohama City, focusing in particular on the two local populations (P5 and P6), to assess the genetic suitability of reinforcement from P6 to P5. MATERIALS AND METHODS 1）Sample We collected eggs or tadpoles of R. japonica from seven populations in Yokohama City (Table 1, Figure 1). Since all wild populations were in nature reserve areas, we minimized the sampling number. Tissue was collected from the tail of tadpoles, and one egg was collected per egg mass. We also collected fingers of male frogs found dead in water pools during breeding season. All samples were stored in 80% ethanol until DNA extraction. DNA was extracted using QIA DNeasy blood and tissue kit (Qiagen) according to the manufacturer’s instruction. 2）Mitochondrial DNA control region Partial DNA sequences of control region in mitochondrial DNA (CR) were amplified according to a previous study [17]. Fig. 1 Location of the seven populations examined in this We used 40 samples of the seven populations (Table 1). DNA study. P1–P7 correspond to the population identification sequences of the PCR product were analyzed in both directions number given in Table 1. － 2 － Genetic variation of Japanese brown frogs in Yokohama City index (Fst) between P5 and P6 were estimated using DnaSP. Population differentiation between the two populations was tested using DnaSP. A median-joining network was constructed using Network [20]. 3）Microsatellite DNA We genotyped 10 types of microsatellite loci using a QIA multiple PCR kit (Qiagen) (Appendix). For genotyping, we used Fig. 2 Median-joining network based on the 563 bp two populations (P5 and P6). Of the 14 samples from P5, we sequences of the mitochondrial control region of the seven haplotypes observed in this study. CR1-CR7 corresponds to the eliminated 5 egg samples as they might have been descendants haplotype identification numbers given in Table 1. Numerals at of the eight adult males. Of the 11 samples from P6, we each node denote the number of differing sequences (one base eliminated one adult male sample as it might have been the if not otherwise specified). parent of 10 egg samples. PCR primers were used according to a previous study [21]. Annealing temperature was set at 57℃. Polymorphism analysis was conducted with the ABI 310 Table 2 Haplotype diversity and nucleotide diversity of genetic analyzer and GeneScan ver. 2.0 (Applied BioSystems) the two populations and the total of 7 populations of Rana japonica in Yokohama City, Kanagawa. according to the manufacturer’ s instructions. Linkage Population Haplotype diversity1） Nucleotide diversity1） disequilibrium and deviation from Hardy-Weinberg equilibrium in the wild populations were tested using Genepop ver. 4.2 [22]. P5 0 0 Expected heterozygosity (He), observed heterozygosity (Ho) P6 0.509 (0.101) 0.00181 (0.00036) and allelic richness were estimated using Fstat 2.9.3.2 [23]. Fst All 0.8 (0.039) 0.0052 (0.00089) between P5 and P6 was estimated using Genepop. Population (P1–P7) differentiation between the two populations was tested using 1） Numbers in parentheses indicate standard deviation. Genepop. To characterize genetic relationships between P5 and P6, STUCTURE (ver. 2.3) [24] was run on the 10 microsatellite DNA for 100,000 Markov chain Monte Carlo (MCMC) cycles 2）Microsatellite DNA polymorphism following 100,000 burn-in cycles, using an admixture model We stably amplified 10 microsatellite loci in 16 samples with independent allele frequencies. Ten replications were (Appendix). From the remaining three wild samples (one performed for each K, in the range K=1–5, and the optimal K sample of P5 and two samples of P6), several loci could not was estimated using STRUCTURE HARVEST [25]. Iterations be amplified in these DNA samples, possibly due to low DNA for the optimal K were analyzed using CLUMPP [26], and quality. No linkage disequilibrium was observed in this study. visualized using DISTRUCT [27]. Based on the polymorphism data of 10 microsatellite loci, Fst between P5 and P6 was estimated at 0.1489 (-0.0794 to RESULTS 0.3207), and they were significantly differentiated (exact G test, 1）Mitochondrial DNA control region df=20, p= 0.000). Structure analysis found that Delta K value Based on sequences of CR (563 bp), we found seven was largest in k=2: 15.45 (k=2), 2.13 (k=3) and 2.01 (k=4). The haplotypes from the 40 samples (Table 1). A median-joining distribution of the alleles in the structure map (k=2) clearly network is shown in Figure 2. From the network, we found two showed that P5 and P6 were differentiated (Figure 3). Number haplogroups, one contained five haplotypes (CR1–CR5) and the of alleles, He, Ho and allelic richness of each microsatellite loci other the remaining two haplotypes (CR6 and CR7).
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