Preliminary study on genetic diversity and phylogenetic relationships of Teropong Temanggung sheep based on mitochondrial cytochrome b sequencesAbstract
The Teropong Temanggung sheep, an indigenous Indonesian breed from Central Java, represents an important genetic resource for smallholder farmers. However, molecular genetic information on this population remains limited. To clarify its maternal genetic background, this preliminary study analyzed the mitochondrial cytochrome b (Cyt b) gene sequence. Blood samples from six (n = 6) Teropong Temanggung sheep were collected, DNA was extracted, and a complete Cyt b gene fragment was amplified and sequenced. Three single-nucleotide polymorphism sites produced two haplotypes. Analysis using MEGA software showed low haplotype diversity (Hd = 0.3333) and nucleotide diversity (Pi = 0.00088). Phylogenetic reconstruction revealed that five samples clustered within haplogroup B and one within haplogroup A, suggesting a mixed maternal lineage origin. These findings provide preliminary baseline information on maternal genetic variation in Teropong Temanggung sheep; however, given the limited sample size and the use of a single mitochondrial marker, they should not be interpreted as evidence of genome-wide genetic distinctiveness. The results serve as a foundation for future studies incorporating larger sample sizes and nuclear genetic markers to better characterize this local sheep population.
Keywords:
Teropong Temanggung sheep; genetic diversity; mitochondrial DNA; cytochrome b gene; phylogenetic relationship; breed conservation
Resumo
A ovelha Teropong Temanggung, uma raça nativa da Indonésia e originária de Java Central, representa um importante recurso genético para pequenos agricultores. No entanto, as informações genéticas moleculares sobre essa população permanecem limitadas. Para esclarecer seu histórico genético materno, este estudo preliminar analisou a sequência do gene mitocondrial citocromo b (Cyt b). Foram coletadas amostras de sangue de seis (n = 6) ovelhas Teropong Temanggung, o DNA foi extraído e um fragmento completo do gene Cyt b foi amplificado e sequenciado. Três locais de polimorfismo de nucleotídeo único produziram dois haplótipos. A análise, utilizando o software MEGA, mostrou baixa diversidade haplotípica (Hd = 0,3333) e diversidade de nucleotídeos (Pi = 0,00088). A reconstrução filogenética revelou que cinco amostras agruparam no haplogrupo B e uma amostra agrupou no haplogrupo A, sugerindo origens de linhagens maternas mistas. Esses achados fornecem informações básicas preliminares sobre a variação genética materna na ovelha Teropong Temanggung; no entanto, devido ao tamanho limitado da amostra e ao uso de um único marcador mitocondrial, esses dados não devem ser interpretados como evidência de distinção genética em todo o genoma. Os resultados servem como base para estudos futuros que incorporem amostras maiores e marcadores genéticos nucleares para caracterizar melhor essa população local de ovinos.
Palavras-chave:
ovelha Teropong Temanggung; diversidade genética; DNA mitocondrial; gene citocromo b; relações filogenéticas; conservação de raças
1. Introduction
Genetic diversity is a fundamental aspect of livestock improvement and conservation because it reflects the evolutionary potential and adaptability of a population (Zhu et al., 2025). Populations with high genetic variability are generally better equipped to respond to environmental changes, diseases, and selective breeding efforts. Conversely, low diversity can increase vulnerability to inbreeding depression and genetic drift, which may threaten the sustainability of local breeds (Biscarini et al., 2015). Information on genetic diversity is essential for developing conservation strategies and utilizing animal genetic resources. Genetic diversity in a population reflects the diversity of its genetic makeup (Selepe et al., 2018). Tools for detecting population diversity, such as mitochondrial DNA, microsatellite DNA, and restricted fragment length polymorphism, have been used at the research level to study and estimate population diversity, calculate genetic distances, and estimate genetic relationships within populations of various local livestock groups, including sheep (Haryono et al., 2014; Satta et al., 2021).
Mitochondrial DNA (mtDNA) has been widely used as a molecular marker to study genetic diversity, population structure, and evolutionary relationships in animals. Unlike nuclear DNA, mtDNA is maternally inherited, does not undergo recombination, and accumulates mutations at a relatively steady rate (Satta et al., 2021; Machova et al., 2022). These features make it ideal for tracing maternal lineages, inferring population structure, and reconstructing phylogenetic relationships. The mtDNA Cytochrome b (Cyt b) gene, being protein-coding and evolutionarily informative, is increasingly favored for genetic diversity studies across various domestic animals, including sheep (Liu et al., 2016; Ibrahim et al., 2023). The Cyt b gene in sheep reveals varying levels of genetic diversity across breeds and regions, such as in Egypt (Othman et al., 2018), Iran (Sofla et al., 2017), and Russia (Koshkina et al., 2021). Recent research across Javanese local sheep breeds exemplifies the value of the mtDNA Cyt b gene for evaluating genetic diversity, haplotype and nucleotide variation, and phylogenetic relationships (Ibrahim et al., 2023).
Indonesia represents a major secondary center of sheep dispersal in Southeast Asia, where livestock were historically introduced through multiple waves of migration and trade, followed by long-term isolation and local adaptation. Java Island, in particular, has become a hotspot for sheep diversification due to its varied agro-ecological zones and long tradition of smallholder-based management systems. These conditions have promoted the formation of region-specific sheep populations that may harbor unique maternal lineages and genetic signatures shaped by both biogeography and domestication history. Therefore, local sheep populations in Java are biologically interesting models for studying micro-evolutionary processes and maternal lineage differentiation.
Teropong Temanggung sheep (Figure 1) are one of the local sheep populations traditionally maintained by farmers in Central Java, particularly in the Temanggung area. Field observations and regional livestock statistics indicate that Teropong Temanggung sheep are commonly preferred by farmers for their ability to survive under smallholder management systems, although systematic evaluations of their productivity and reproductive performance remain limited. Therefore, any perceived adaptability or resilience should be regarded as observational rather than empirically quantified. To date, Teropong Temanggung sheep have not been genetically characterized using mitochondrial markers. This study reports the first mtDNA Cyt b–based genetic diversity of Teropong Temanggung sheep and provides a comparative assessment with geographically adjacent Indonesian sheep populations. The objective of this study was to characterize the maternal genetic diversity, haplotype composition, and phylogenetic position of Teropong Temanggung sheep based on the mtDNA Cyt b gene, thereby providing a molecular baseline to support future breed recognition and conservation planning.
2. Materials and Methods
2.1. Ethical approval
Temanggung sheep were used in this study in compliance with research procedures that were examined, authorized, and validated by the Ethical Clearance Commission of the Faculty of Veterinary Medicine, Universitas Gadjah Mada (No. 127/EC-FKH/Int./2024).
2.2. Sample collection
A total of six (n = 6) clinically healthy Teropong Temanggung sheep were sampled from several villages in the Temanggung Regency, Central Java, Indonesia (7°15′56″S 110°12′59″E). Animals were selected using a purposive sampling approach, which intentionally selects unrelated adult individuals from different household flocks to minimize close kinship among sampled animals. Approximately 2 mL of whole blood was collected aseptically from the jugular vein using sterile 3-cc syringes and transferred into vacutainer tubes containing ethylenediaminetetraacetic acid (EDTA). Samples were transported to the laboratory in a cooler box maintained at approximately 4 °C and subsequently stored at –20 °C until DNA extraction. Sampling was carried out from April to November 2024. Laboratory analyses were performed at the Tropical Animal Research Center, Faculty of Animal Science, Universitas Gadjah Mada, and at the Whole Genome Sequencing Laboratory of the National Research and Innovation Agency (BRIN), Indonesia.
2.3. DNA isolation and amplification of Cyt b
DNA isolation was performed following the Geneaid gSYNC™ DNA Extraction Kit Quick Protocol (Geneaid Biotech, Taiwan). The DNA isolation process included cell lysis, DNA binding, washing, and elution. The mitochondrial cytochrome b (Cyt b) gene was amplified using the forward primer Alek-CBF: 5′-CAACCCCACCACTTACAA-3′ and reverse primer Alek-CBR: 5′-CCTTGAGTCTTAGGGAGGTT-3′ (Ibrahim et al., 2023), producing an expected amplicon size of 1,409 bp (Ibrahim, 2021). Each 50 µL PCR reaction contained 2 µL of DNA template, 25 µL of MyTaq™ HS PCR Mix (Bioline, UK), 2 µL of each primer, and 19 µL of nuclease-free water.
The protocol began with a 10-minute pre-denaturation at 95 °C, followed by 35 cycles, each consisting of denaturation at 95 °C for 30 s, primer annealing at 60 °C for 30 s, extension at 72 °C for 90 s, then ending with a final extension at 72 °C for 10 min, and storage at 4 °C. The PCR product was visualized using a 1.5% agarose gel, and electrophoresis was run at 100 V for 40 min. The amplification result was visible under the ultraviolet illuminator. Purified PCR products were sequenced using bidirectional Sanger sequencing at the Whole Genome Sequencing Laboratory, National Research and Innovation Agency (BRIN), Indonesia.
2.4. Data analyses
The sequencing results were analyzed using the Molecular Evolutionary Genetic Analysis (MEGA) software version 12 (Kumar et al., 2024). The sequence alignment was performed using the Clustal W method. The nucleotide genetic distances were analyzed using the Pairwise distance method and the Kimura 2-parameter model. Phylogenetic trees were constructed using the Maximum Likelihood (ML) method with 1000 bootstrap replicates under the Kimura 2-parameter model to assess topology robustness. Phylogenetic analyses included reference sequences of known haplogroups of domestic sheep (Ovis aries), wild sheep (Davenport et al., 2018; Deng et al., 2020; Dotsev et al., 2019; Dotsev et al., 2025; Lv et al., 2015; Meadows et al., 2011; Rezaei et al., 2010; Sanna et al., 2015; Wang et al., 2019) from NCBI GenBank, as well as Indonesian local sheep breeds (Meadows et al., 2005; Ibrahim, 2021; Ibrahim et al., 2023) (Table 1).
Reference Cyt b sequences of Indonesian sheep, the known haplogroups of domestic sheep (Ovis aries), and wild sheep.
3. Results
3.1. Nucleotide and haplotype diversity of the Cyt b gene in Teropong Temanggung sheep
The nucleotide base composition of the cytochrome b gene in Teropong Temanggung sheep showed that adenine (A) was the most abundant base at 31.4%, followed by cytosine (C) at 28.6%, thymine (T) at 27.0%, and guanine (G) at 13.0%. The overall C+G content was 41.6%, which indicates an A+T bias (58.4%) in the mitochondrial genome. Polymorphism data of complete mtDNA Cyt b gene sequences in Temanggung sheep are provided in Table 2.
The analysis of the complete mtDNA Cyt b gene sequence (1,140 bp) from six Teropong Temanggung sheep samples revealed 1,137 monomorphic sites and three polymorphic singleton sites at positions 309 (C>T), 495 (G>A), and 828 (C>T). The nucleotide diversity (Pi) was 0.00088±0.00057, and the average number of nucleotide differences (k = 1.000), indicating high sequence similarity among sampled individuals. Two haplotypes were identified from the three variable sites, with haplotype diversity (Hd) of 0.3333±0.0463 (bootstrap 95% CI = 0.000–0.733). Haplotype 1 included five samples (JF1, JF2, PF14, WF11, and WF14), while haplotype 2 contained a single sample (PF15). Haplotype 2 of Teropong Temanggung sheep shared an identical nucleotide sequence with sheep of Haplogroup A, whereas haplotype 1 closely matches Haplogroup B, differing only at position 828 (C>T) (Table 3).
Single-nucleotide polymorphism (SNP) of the complete Cyt b gene in the Teropong Temanggung sheep and the known Ovis aries haplogroup.
3.2. Genetic distance and phylogenetic tree based on the Cyt b gene
The genetic distance values between Teropong Temanggung sheep and the known haplogroup Ovis aries, based on mtDNA Cyt b sequences, are presented in Table 4. The closest genetic distance is observed between Teropong Temanggung sheep and sheep with haplogroup B (0.00102), followed by haplogroup A (0.00220), haplogroup E (0.00797), haplogroup D (0.00871), and the farthest being haplogroup C (0.01020). Phylogenetic reconstruction (Figure 2) showed that five of six Teropong Temanggung sheep (83.33%) clustered within haplogroup B, while one individual (16.67%) clustered within haplogroup A. In contrast, haplogroups C, D, and E formed more distant clades.
Genetic distances (below) and standard error (above) among Teropong Temanggung sheep and the haplogroup reference of domestic sheep.
Phylogenetic tree (Maximum Likelihood method with 1000x bootstrap) of Teropong Temanggung sheep and reference of local Indonesian sheep (Ibrahim et al., 2023), known haplogroup domestic sheep, and wild sheep based on mtDNA Cyt b gene sequences.
4. Discussion
Variation in the mitochondrial Cyt b gene primarily reflects maternal lineage structure rather than individual genetic potential or complex quantitative traits, which are largely determined by nuclear genomic variation and management practices. Therefore, Cyt b is mainly used to infer maternal ancestry, population structure, and historical dispersal patterns, but it does not capture genome-wide diversity or performance-related genetic variation. Consequently, results derived from this marker should be interpreted as lineage-level rather than individual-level genetic information.
Based on the DNA diversity of the Cyt b gene in Teropong Temanggung sheep, an overview of maternal lineage diversity, phylogenetic placement, and genetic relationships among sampled individuals can be obtained. Based on the results of sequencing and alignment of the Cyt-b gene in Teropong Temanggung sheep and local sheep on Java Island (Javanese Fat-Tailed, Wonosobo, Batur, Priangan, and Garut sheep) (Ibrahim, 2021; Ibrahim et al., 2023) and other sheep species taken from the GenBank database, a complete Cyt b gene sequence of 1,140 bp was obtained. The nucleotide composition in this study is consistent with the general characteristics of animal mitochondrial DNA, which typically shows a higher proportion of A and T nucleotides than G and C (Lavrov and Pett, 2016).
The nucleotide and haplotype diversity in this study was lower than that reported by Ibrahim et al. (2023) for Javanese sheep breeds (Hd = 0.54, Pi = 0.00119), which formed six distinct haplotypes and clustered into two primary haplogroups (A and B). Despite nucleotide variations, no amino acid changes were observed in Teropong Temanggung sheep, indicating a high degree of sequence conservation in the Cyt b region among sampled individuals. The presence of two haplotypes suggests limited maternal lineage variation within the sampled animals.
Haplogroup B dominates in European sheep, while haplogroup A is prevalent in Asian sheep, but both are present in both regions due to historical migrations and introgression (Hussain and Erdoğan, 2021; Machová et al., 2022). The present results indicate that the maternal ancestry of Teropong Temanggung sheep is shared with haplogroups A and B, rather than demonstrating direct evidence of recent crossbreeding or introgression, which would require additional nuclear genomic data. The clustering pattern in the phylogenetic tree also reveals that Teropong Temanggung sheep are genetically closer to local Indonesian breeds, particularly those belonging to haplogroups A and B, while having limited genetic contribution from haplogroups C and D. This pattern may reflect historical dispersal and localized breeding practices in Central Java; however, this interpretation remains a hypothesis in the absence of detailed records on breeding management, animal movement, and barriers to gene flow in the Teropong Temanggung region. Low mtDNA diversity observed in this study does not necessarily indicate low genome-wide diversity or high inbreeding, because mitochondrial markers represent only the maternal lineage and constitute a very small fraction of the genome. Therefore, conclusions regarding inbreeding status and overall genetic health cannot be drawn solely from Cyt b data. Nevertheless, the dominance of haplogroup B among the sampled individuals suggests that this maternal lineage is common in the Temanggung area; however, comparative frequency data from nearby Central Java sheep populations are required to contextualize whether this pattern is unique or typical of the region.
The present findings primarily provide baseline information on maternal lineage composition rather than direct evidence for breeding value, performance, or adaptation (Cao et al., 2021; Ceccobelli et al., 2023; Justinski et al., 2023; Nanaei et al., 2024). Any potential associations between mtDNA haplogroups and production, adaptation, or resilience traits remain speculative and should be considered hypotheses for future studies that integrate phenotypic data and genome-wide nuclear markers (Adeniyi et al., 2022; Lv et al., 2022; Rochus et al., 2018). Overall, this preliminary study provides baseline maternal lineage information for Teropong Temanggung sheep and highlights important knowledge gaps that require further investigation using larger sample sizes, phenotypic characterization, and multi-locus or genome-wide genetic approaches.
Given the small sample size and reliance on a single mitochondrial marker, the present results should be interpreted as preliminary. Future studies incorporating nuclear genomic markers, larger population sampling, and production and adaptation data will be essential to support breed development and conservation planning at the local and national levels in Indonesia.
5. Conclusion
This preliminary/pilot study characterized the maternal genetic variation of Teropong Temanggung sheep using the mitochondrial Cyt b gene. Two maternal haplotypes belonging to haplogroups B and A were identified, indicating a mixed maternal origin within the sampled individuals. The low mtDNA diversity observed reflects variation only within maternal lineages and does not reflect genome-wide genetic diversity or inbreeding status. Therefore, the present findings should be interpreted as baseline maternal-lineage information rather than evidence for production performance, adaptation, or disease resistance. Future research should include expanded population sampling, integration of nuclear genetic markers (e.g., microsatellites or genome-wide SNPs), and incorporation of morphological, production, and management data to enable comprehensive breed characterization and support conservation and development strategies for Teropong Temanggung sheep at the local and national levels in Indonesia.
Acknowledgements
The authors acknowledge the facilities, scientific and technical support from the Tropical Animal Research Center, Faculty of Animal Science UGM, and the Whole Genome Sequencing Laboratory, National Research and Innovation Agency through E-Layanan Sains, Badan Riset dan Inovasi Nasional. This project was financed by Universitas Gadjah Mada Doctoral Competency Improvement Program, with Assignment Letter: 6541/UN1.P1/PT.01.03/2024 and announcement of project funding: 6514/UN1.P1/PT.01.01/2024.
Data Availability Statement
The research data are available from the corresponding author on reasonable request.
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Editor:
Takako Matsumura Tundisi
