Next Article in Journal
Genome Insight and Description of Previously Uncultured N2-Fixing Bacterium Rhizobium terricola sp. nov., Isolated from Forest Rhizospheric Soil by Using Modified Culture Method
Previous Article in Journal
Review of the Cyanobacterial Genus Phormidesmis (Leptolyngbyaceae) with the Description of Apatinema gen. nov.
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Diversity
Volume 14
Issue 9
10.3390/d14090732
diversity-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Genetic Diversity and Relatedness of Group-Living Small Mammals on the Mongolian Plateau

by
Guiming Wang
1,
Xinrong Wan
2,*,
Wei Liu
2 and
Xueyan Shan
3
1
Department of Wildlife, Fisheries and Aquaculture, Mail Stop 9690, Mississippi State University, Mississippi State, MS 39762, USA
2
Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China
3
Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(9), 732; https://doi.org/10.3390/d14090732
Submission received: 19 August 2022 / Revised: 1 September 2022 / Accepted: 3 September 2022 / Published: 6 September 2022
(This article belongs to the Section Biodiversity Loss & Dynamics)
Browse Figures
Versions Notes

Abstract

:
Genetic diversity plays an important role in the evolution and adaptation of organisms. Losses of genetic diversity make organisms more vulnerable to climate changes and diseases, reducing the viability of small populations. In addition to natural selection, genetic drift, dispersal, inbreeding, and population bottleneck, the social systems of animals may also affect the genetic diversity of populations. We aimed to test the hypothesis that the delayed dispersal of group-living small mammals would reduce genetic diversity through attenuated gene flow but enhance genetic relatedness. We used microsatellite analysis to estimate genetic diversity and the Queller and Goodnight relatedness coefficients of Daurian pikas (Ochotona dauurica) and Mongolian gerbils (Meriones unguiculatus), two socially monogamous small mammals living in social groups in Inner Mongolia, China. The average genetic relatedness of social groups was inversely related to the average genetic diversity of social groups in Daurian pikas but not in Mongolian gerbils, partially supporting our hypothesis. Dispersal following frequent local extinctions resulted in the recolonization of burrow systems by individuals with different genetic makeups, increasing genetic diversity and reducing the genetic relatedness of the social groups of Daurian pikas. On the other hand, delayed short-distance dispersal was sufficient to maintain the high genetic diversity and high genetic relatedness of gerbil social groups independently.

1. Introduction

Genetic diversity is the raw material of natural selection and determines the adaptation of species to environmental changes [1,2]. High genetic diversity improves the resistance of species to diseases and the viability of small populations [2,3,4]. Therefore, genetic diversity is an integral component of biodiversity. Genetic diversity is primarily affected by natural selection, genetic drift, gene flow via dispersal (or migration), population bottleneck, and reproduction mode [2,5]. Life history traits may also affect genetic diversity by influencing effective population sizes [5].
Social systems of animals such as mating systems and social organization may influence the effective population size (e.g., through the deviation from equal reproductive contributions and changes in sex ratio) and dispersal [5]. Social organization can exert significant effects on the genetic diversity of social organisms. For instance, the delayed dispersal of juveniles forms social groups, increasing genetic relatedness within social groups [6]. Kinship, or genetic relatedness, is a key factor influencing the evolution of social groups [7]. Inclusive fitness through kinship or genetic relatedness promotes the formation and maintenance of group living when the indirect benefits of delayed natal dispersal or living in groups outweigh the costs of group living [7]. It is plausible to predict an inverse relationship between genetic relatedness and genetic diversity unless gene flow between social groups enhances genetic diversity. On the other hand, group-living rodents like Mongolian gerbils (Meriones unguiculatus) may exhibit group territoriality to defend against immigration or even those merely passing through their territories [8,9]. Such territoriality may become a social barrier to gene flow (i.e., isolation by social resistance) [10]. It is unknown whether kinship-based group living results in similar relationships between genetic diversity and the relatedness of social groups in different species.
The Daurian pika (Ochotona dauurica) and Mongolian gerbils are two group-living small mammals commonly found in the grassland on the Mongolian Plateau [11,12]. Daurian pikas are believed to be socially monogamous [13] and reproduce from April to August [14,15]. Unlike the pikas in North America [13], Daurian pikas live in social groups year-round [11]. A social group consists of 2–5 individuals in Inner Mongolia (G.M. Wang, personal observation). Populations of Daurian pikas undergo frequent local extinctions during winter [16], which makes it difficult to conduct long-term studies of the behavior and population of this species. It is possible that the dispersal and recolonization of burrow systems by different individuals with different genetic makeups result in an inverse relationship between the genetic relatedness and genetic diversity of Daurian pika social groups. To the best of our knowledge, little is known about the genetic relatedness and genetic diversity of the social groups of Daurian pikas.
Mongolian gerbils are social rodents distributed on the typical steppes, desert grasslands, and agricultural fields on the Mongolian Plateau [12]. Mongolian gerbils also live in groups, each consisting of 2–17 individuals possibly as an extended family group [17,18]. Mongolian gerbils are also believed to be socially monogamous [19]. Juvenile gerbils often delay their natal dispersal, remaining at their natal sites after weaning [17,20]. The average genetic relatedness of the social groups of Mongolian gerbils is 0.28 (95% CI: 0.23–0.34), and dispersal between social groups results in a significant spatial population genetic structure [6]. However, relationships between the genetic diversity and relatedness of Mongolian gerbil social groups remain unknown. Furthermore, it is unclear whether a similar group-living behavior results in similar genetic diversity–relatedness relationships between Daurian pikas and Mongolian gerbils.
In this work, we tested the hypothesis that the delayed dispersal of group-living small mammals reduces genetic diversity through the attenuation of gene flow but enhances genetic relatedness, resulting in an inverse relationship between genetic diversity and relatedness. Alternatively, we hypothesized that gene flow or dispersal between social groups is sufficient to maintain sufficiently high genetic diversity in the social groups of small mammals, with the genetic diversity of social groups being independent of genetic relatedness. We carried out a microsatellite analysis of the genetic diversity and relatedness of Daurian pikas. We also reanalyzed the microsatellite genetic data of Mongolian gerbils from Wang, Liu, Wang, Zhong, and Wan [6] to test the two hypotheses.

2. Methods

2.1. Study Areas

We carried out a capture–recapture study of Daurian pikas in Naren, Abaga Banner (county), in the grassland of northcentral Inner Mongolia, China (44°26′ N, 114°58′ E, 1130 m elevation). The climate is semi-arid, with mean annual total precipitation ranging from 135.0 to 267.2 mm. Monthly mean temperatures varied from −22.9 to 23.6 °C. Snow cover lasted from mid-to-late October to early May. Vegetation on the study site mainly consisted of Leymus chinense, Artemisia frigid, Allium polyrhizum, Salsola collina, and Chenopodium glaucum [21].
We reanalyzed the microsatellite genetic data of Mongolian gerbils from Wang, Liu, Wang, Zhong, and Wan [6] to test the two alternative hypotheses. We live-trapped Mongolian gerbils at Xima Gou (115°22′ E, 42°07′ N, 1450 m elevation), located in a typical steppe intermixed with the semi-arid climate cropland in Taipusi Qi (county), Inner Mongolia, China. Average monthly temperature ranged from −19.1 to 21.1 °C. Average annual total precipitation ranged from 258 to 550 mm [22]. Daurian pikas and Mongolian gerbils coexist in our study areas [12].

2.2. Live-Trapping of Daurian Pikas and Mongolian Gerbils

We live-trapped Daurian pikas biweekly on a 1.5 ha plot (140 m × 110 m) from 12 May 2010 to 28 October 2010; from 10 July 2011 to 11 October 2011; and from 20 May 2012 to 5 October 2012. We did not trap Daurian pikas during winter to avoid trap mortality resulting from low temperatures [21]. Our trapping plot had 30 Daurian pika burrow systems. We placed a wire-mesh live trap (28 cm × 13 cm × 10 cm) at each active burrow entrance in each of the 30 burrow systems, with 8–12 traps per burrow system and a total of 350–400 traps each trapping week. We live-trapped Daurian pikas from 0500 h to 1900 h, with traps being closed from 1100 h to 1500 h to avoid trap mortality resulting from heat stress from June to August. Traps were checked every one or two hours. In May, September, and October, the months of lower temperatures, living-trapping was carried out from 0630 h to 1730 h to avoid trap mortalities due to extremely low temperatures in the early morning and late afternoon during those months [21].
Each captured pika was marked with an ear tag with a unique identification (ID) number (S. Roestenburg Inc., Herriman, UT, USA) upon its initial capture. We also sexed captured pikas and weighed them to the nearest 0.1 g with a portable electronic scale (Scout SE601F, Ohaus Corp., Parsippany, NJ, USA). The ID number, trap location (i.e., burrow system ID), sex, and body mass of each capture were recorded. We cut a small piece (2 mm × 2 mm) of ear biopsy from each captured pika for DNA extraction. Captured pikas were released at the same trap stations of the captures immediately after handling.
Our trapping plot of Mongolian gerbils was situated on a 9 ha grassland (300 m × 300 m) surrounded by wheat (Triticum spp.) and cabbage (Brassica spp.) crop fields. The vegetation was dominated by the grass Leymus chinense and the herb Corispermum mongolicum and included a mixture of grasses such as Cleistogenes squarrosa and Setaria viridis; the herbs Artemisia sieversiama, Artemisia scoparia, and Heteropappus altaicus; and the small shrubs Caragana microphylla and C. korshinskii. We live-trapped Mongolian gerbils from 28 burrow systems using the same capture-recapture methods as those for trapping Daurian pikas from 28 April to 21 October in 2006 at 2-week intervals [22]. We clipped 1 toe per foot, removing half a toe at the joint with a pair of sharp, thin-bladed scissors from each captured gerbil for the microsatellite DNA analyses [6].

2.3. Microsatellite Analysis

We extracted genomic DNA from the ear tissue samples of captured pikas using phenol–chloroform extraction methods after Sambrook and Russell [23]. The quality and quantity of extracted DNA were visually examined on agarose gels stained with ethidium bromide. We used cross-species amplifications of 11 microsatellite markers to genotype captured pikas with polymerase chain reactions (PCR). Of the 11 markers, ocp1, ocp2, ocp3, and ocp5 were originally developed for O. princeps [24]; occ02 for O. collaris [25]; and p7F, p47F, p124R, p149F p156F, and p172F for O. curzoniae [26]. We used the same PCR reaction conditions and protocol for each marker as in Peacock, Kirchoff, and Merideth [24]; Li, Geng, Yang, Zhang, and Hu [26]; and Zgurski, Davis, and Hik [25]. Amplified fragments were electrophoresed on an ABI PRISM 377 automated sequencer (Applied Biosystems, Foster City, CA, USA), and were scored using Genescan® Version 3.7 (Applied Biosystems). We genotyped each pika sample twice independently to assess typing error rates. If differences occurred between two genotyping runs, we continued genotyping until a consensus was reached. We assessed null alleles, short allele dominance, and typing errors associated with stutter using the program MICRO-CHECKER [27]. We tested the Hardy–Weinberg equilibrium (HWE) at each locus and linkage disequilibrium (LD) between each pair of loci using the program GENEPOP 3.4 with the Markov chain option of 50 batches and 100,000 iterations per batch [28]. We used the Bonferroni correction for multiple comparisons with a nominal significance level of 0.05 in the LD assumption test.
We extracted DNA from the toe tissues of gerbils using the same phenol–chloroform extraction methods. We visually examined the quality and quantity of extracted DNA on agarose gels stained with ethidium bromide. We genotyped 327 gerbils from 28 social groups using nine microsatellite markers, Mungµ1, Mungµ2, Mungµ3, Mungµ4, Mungµ5, Mungµ6, Mungµ7, Mungµ8, and Mungµ9 [29]. We assessed genotyping errors and tested the HWE and LD assumptions using the same methods as those for Daurian pikas (see [6] for details).
We defined a social group as the individual Daurian pikas or Mongolian gerbils that were live-captured in the same burrow system. We calculated the mean numbers of alleles per locus, average observed and expected heterozygosity at each locus, average Shannon diversity index, and mean pairwise Queller and Goodnight (QG) relatedness coefficients [30] with 999 iterations by social group using the program GENALEX 6.4 [31]. We used the Shannon diversity index as the genetic diversity index for the social groups of Daurian pikas and Mongolian gerbils.

2.4. Statistical Analysis

We used the linear regression of the average Shannon diversity index against mean the QG relatedness coefficient to test our hypothesis that the average genetic diversity of social groups decreases with increased genetic relatedness due to delayed dispersal. We used R v. 4.2.0 to carry out the linear regression [32].

3. Results

All 11 microsatellite loci were successfully cross-amplified in 194 Daurian pikas. The HWE at each locus and LD assumptions were met at a significance level of 0.05 with the Bonferroni correction in 30 social groups of Daurian pikas. The genetic diversity of the microsatellite loci was high with the expected heterozygosity ( H e ) ranging from 0.55 to 0.93 (Table 1). The Shannon diversity index of microsatellite genetic diversity was inversely related to the average QG genetic relatedness coefficient of the Daurian social groups (slope = −1.09, p = 0.02, df = 24, R 2 = 0.21, Figure 1a). However, genetic diversity was not related to the average genetic relatedness of the Mongolian gerbil social groups (slope = 0.35, p = 0.78, df = 24, R 2 = 0.003, Figure 1b). Social groups of Mongolian gerbils consisted of more related individuals than did those of the Daurian pika social groups (t = −4.0412, df = 38, p = 0.0003, Figure 2a,b).

4. Discussion

The genetic diversity of Daurian pikas in central Inner Mongolia was high, with highly polymorphic microsatellite loci. More than 50% of the burrow systems were occupied by non-kin, with the QG relatedness coefficient being negative, suggesting that the inhabitants of those burrow systems were less related in ancestry than the average [33], whereas social groups of Mongolian gerbils were kin-based (r > 0), with 36% of Mongolian gerbil social groups being first cousins (r = 0.125) and half-siblings (r = 0.25) [34]. Furthermore, our findings support the hypothesis that increases in genetic diversity reduce genetic relatedness in Daurian pikas but not in Mongolian gerbils. Therefore, the formation and dynamics of Daurian pika social groups may be different from those of Mongolian gerbils.
The Daurian pika population we genotyped exhibited stable survival probabilities and a slight decline in relative abundance from 2010 to 2012 [21]. The average expected heterozygosity ( H e   = 0.55–0.93) of the microsatellite loci was higher ( H e   = 0.42–0.69) than that of a declining population of American pikas (O. princeps) in Oregon, United States [35], and that ( H e   = 0.59–0.65) of a fluctuating collared pika (O. collaris) population in Yukon, Canada [36]. Likewise, the genetic diversity of Daurian pika populations was higher than that of plateau pikas (O. curzoniae) in the Qinghai–Tibet Plateau, China [37]. Despite high genetic diversity, the observed heterozygosity of microsatellite loci tended to be lower than the expected heterozygosity, suggesting some level of inbreeding in Duarian pikas (Table 1). Daurian pika populations undergo frequent local extinctions, exhibiting dramatic population fluctuations [16]. For instance, Daurian pikas disappeared within a few hundred kilometers in our study regions after 2014 (G. Wang, personal observation). Daurian pika populations may maintain their high genetic diversity when a population colonizes a new habitat by mixing individuals of different genetic makeups.
Daurian pikas do not appear to excavate their burrow systems [11]. Daurian pikas outcompete Brandt’s voles (Lasiopodomys brandtii) for space and often overtake the burrow systems of Brandt’s voles [11]. Contrary to the kin-based composition of Mongolian gerbil social groups, more than 50% of Daurian pika social groups (i.e., pikas inhibiting the same burrow system) consisted of non-kin group mates with negative QG relatedness coefficients. We propose two hypotheses to explain this observation. First, a family-based social group of Daurian pikas often consists of 3–4 Daurian pikas [38]. Daurian pikas from different family groups may colonize a burrow system to form a social group with high genetic diversity and low genetic relatedness (Figure 1a and Figure 2a). This finding is consistent with the frequent local extinction and recolonization of Daurian pika populations in Inner Mongolia [16,21]. Octodon degus, a group-living rodent, also lacks a kin structure with lower genetic relatedness due to the high turnover of group members [39]. It is uncertain whether juvenile Daurian pikas delay their natal dispersal, which increases the genetic relatedness of social groups. Second, Daurian pikas that were captured in a burrow system over three years may belong to different families that successively colonized the same burrow system at different times. Similarly, different social groups of the group-living rodent tuco-tuco (Ctenomys sociabilis) occupy the same burrow systems in different years [40]. Therefore, the higher genetic diversity and lower genetic relatedness of Daurian pika social groups might be caused by the dispersal and recolonization of the same burrow systems by different family groups of different genetic makeups.
The genetic diversity of Mongolian gerbils on the typical steppe of Inner Mongolia ( H e = 0.81–0.9, this study) is higher than that of wild populations in the periphery of its range ( H e = 0.41, Yinchuan, Ningxia, China; H e   = 0.39, Hohhot, Inner Mongolia, China) [41]. Mongolian gerbils have an ecological lifetime of 6–9 months, with most adults dying over winter [9,22,42]. The juvenile gerbils often disperse a short distance to gain reproductive opportunities and avoid inbreeding [6]. It is possible that a high genetic diversity of Mongolian gerbil social groups is maintained by dispersal. The effective dispersal distance of Mongolian gerbils is about 60–70 m, with genetic relatedness decreasing from 0.2 to 0.0 [43]. The distance between two burrow systems of Mongolian gerbils ranges from 18 m to 280 m [6]. Gray mouse lemurs (Microcebus murinus) form social or communal groups during the daytime [44]. The female lemurs have higher-than-average genetic relatedness, but they do not have any sign of inbreeding due to male dispersal [44]. The high genetic relatedness of Mongolian gerbil social groups is possibly caused by delayed dispersal or short-distanced dispersal, which is adequate to maintain the genetic diversity of social groups.
Daurian pikas are a keystone species on the Mongolian Plateau [45]. The Mongolian gerbil is a rodent species of economic and public health importance [14]. Our results demonstrate the high genetic diversity of both Daurian pikas and Mongolian gerbils and the potential effects of sociality on population genetic structure. However, future studies are needed to elucidate the mechanisms and roles of dispersal in the maintenance of the genetic diversity of the two species, which both exhibit frequent local extinctions and recolonizations.

Author Contributions

Conceptualization, G.W., X.W. and X.S.; methodology, G.W., W.L. and X.S.; formal analysis, G.W. and X.S.; writing—original draft preparation, G.W.; writing—review and editing, X.W., W.L. and X.S. All authors have read and agreed to the published version of the manuscript.

Funding

Guiming Wang was financially supported by the Forest and Wildlife Research Center of Mississippi State University.

Institutional Review Board Statement

Our trapping and handling of Daurian pikas were approved by the Institutional Animal Use and Care Committee (IACUC) of the Institute of Zoology, the Chinese Academy of Sciences, and the Mississippi State University IACUC (protocol 11-031). Our trapping and handling of Mongolian gerbils were approved by the Institutional Animal Use and Care Committee of the Institute of Zoology, Chinese Academy of Sciences.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study will be openly available in a public repository after the manuscript is accepted for publication.

Acknowledgments

We thank Lijun Chen, Bing Xue, and Yongzhi Su for their assistance in fieldwork.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Hughes, A.R.; Inouye, B.D.; Johnson, M.T.; Underwood, N.; Vellend, M. Ecological consequences of genetic diversity. Ecol. Lett. 2008, 11, 609–623. [Google Scholar] [CrossRef] [PubMed]
  2. Freeland, J.R. Molecular Ecology; Wiley: West Sussex, UK, 2005. [Google Scholar]
  3. Reed, D.H.; Frankham, R. Correlation between fitness and genetic diversity. Conserv. Biol. 2003, 17, 230–237. [Google Scholar] [CrossRef]
  4. Frankham, R.; Ballou, S.E.J.D.; Briscoe, D.A.; Ballou, J.D. Introduction to Conservation Genetics; Cambridge University Press: Cambridge, UK, 2002. [Google Scholar]
  5. Ellegren, H.; Galtier, N. Determinants of genetic diversity. Nat. Rev. Genet. 2016, 17, 422–433. [Google Scholar] [CrossRef]
  6. Wang, Y.; Liu, W.; Wang, G.; Zhong, W.; Wan, X. Genetic consequences of group living in Mongolian gerbils. J. Hered. 2011, 102, 554–561. [Google Scholar]
  7. Hamilton, W.D. Genetical evolution of social behaviour I. J. Theor. Biol. 1964, 7, 17–52. [Google Scholar] [CrossRef]
  8. Agren, G.; Zhou, Q.; Zhong, W. Territoriality, cooperation and resource priority: Hoarding in the Mongolian gerbil, Meriones unguiculatus. Anim. Behav. 1989, 37, 28–32. [Google Scholar] [CrossRef]
  9. Liu, W.; Wang, G.; Wan, X.; Zhong, W. Effects of supplemental food on the social organization of Mongolian gerbils during the breeding season. J. Zool. 2009, 278, 249–257. [Google Scholar] [CrossRef]
  10. Armansin, N.C.; Stow, A.J.; Cantor, M.; Leu, S.T.; Klarevas-Irby, J.A.; Chariton, A.A.; Farine, D.R. Social barriers in ecological landscapes: The social resistance hypothesis. Trends Ecol. Evol. 2020, 35, 137–148. [Google Scholar] [CrossRef]
  11. Wang, G.; Zhou, Q.; Zhong, W.; Wang, Z. Spatial overlap between sympatric Microtus brandti (Rodentia, Microtinae) and Ochotona daurica (Lagomorpha, Ochotonidae) in the steppes of inner Mongolia. Mammalia 2003, 67, 349–354. [Google Scholar] [CrossRef]
  12. Wang, G.; Zhong, W. Mongolian gerbils and Daurian pikas responded differently to changes in precipitation in the Inner Mongolian grasslands. J. Arid Environ. 2006, 66, 648–656. [Google Scholar] [CrossRef]
  13. Smith, A.T. Patterns of pikas (Genus Ochotona) life history variation. In Evolution of Life Histories of Mammals; Boyce, M.S., Ed.; Yale University Press: New Haven, CT, USA, 1988; pp. 233–256. [Google Scholar]
  14. Zhong, W.; Wang, G.; Zhou, Q.; Wan, X. Effects of winter food availability on the abundance of Daurian pikas (Ochotona dauurica) in Inner Mongolian grasslands. J. Arid Environ. 2008, 72, 1383–1387. [Google Scholar] [CrossRef]
  15. Chen, L.J.; Zhang, W.J.; Zhang, X.Q.; Jia, J.J.; Liu, W.; Wan, X.R. A preliminary study of reproductiive ecology of Daurian pikas in the typica steppe. Chin. J. Zool. 2014, 49, 649–656. [Google Scholar]
  16. Formozov, A.N. Adaptive modifications of behavior in mammals of the Eurasian steppes. J. Mammal. 1966, 47, 208–223. [Google Scholar] [CrossRef]
  17. Agren, G.; Zhou, Q.; Zhong, W. Ecology and Social-Behavior of Mongolian Gerbils, Meriones unguiculatus, at Xilinhot, Inner-Mongolia, China. Anim. Behav. 1989, 37, 11–27. [Google Scholar] [CrossRef]
  18. Wang, Y.; Liu, W.; Wang, G.; Wan, X.; Zhong, W. Home-range sizes of social groups of Mongolian gerbils Meriones unguiculatus. J. Arid Environ. 2011, 75, 132–137. [Google Scholar] [CrossRef]
  19. Scheibler, E.; Weinandy, R.; Gattermann, R. Social categories in families of Mongolian gerbils. Physiol. Behav. 2004, 81, 455–464. [Google Scholar] [CrossRef]
  20. Clark, M.M.; Galef, B.G. Socially induced infertility: Familial effects on reproductive development of female Mongolian gerbils. Anim. Behav. 2001, 62, 897–903. [Google Scholar] [CrossRef]
  21. Chen, L.; Wang, G.; Wan, X.; Liu, W. Complex and nonlinear effects of weather and density on the demography of small herbivorous mammals. Basic Appl. Ecol. 2015, 16, 172–179. [Google Scholar] [CrossRef]
  22. Liu, W.; Wang, G.; Wang, Y.; Zhong, W.; Wan, X. Population ecology of wild Mongolian gerbils Meriones unguiculatus. J. Mammal. 2009, 90, 832–840. [Google Scholar] [CrossRef]
  23. Sambrook, J.; Russell, D.W. Molecular Cloning: A Laboratory Manual, 3rd ed.; Cold Spring Harbor Laboratory Press: Cold Spring, NY, USA, 2001. [Google Scholar]
  24. Peacock, M.M.; Kirchoff, V.S.; Merideth, S.J. Identification and characterization of nine polymorphic microsatellite loci in the North American pika, Ochotona princeps. Mol. Ecol. Notes 2002, 2, 360–362. [Google Scholar] [CrossRef]
  25. Zgurski, J.M.; Davis, C.S.; Hik, D.S. Isolation and characterization of microsatellite loci for the collared pika (Ochotona collaris) and their cross-amplification in five other Ochotona species. Mol. Ecol. Resour. 2009, 9, 867–871. [Google Scholar] [CrossRef] [PubMed]
  26. Li, K.X.; Geng, J.N.; Yang, J.; Zhang, Y.M.; Hu, S.N. Isolation and characterization of 13 microsatellite loci in the plateau pika (Ochotona curzoniae). Conserv. Genet. 2009, 10, 785–787. [Google Scholar] [CrossRef]
  27. Van Oosterhout, C.; Hutchinson, W.F.; Wills, D.P.M.; Shipley, P. MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 2004, 4, 535–538. [Google Scholar] [CrossRef]
  28. Raymond, M.; Rousset, F. GENEPOP (Version-1.2): Population genetics software for exact tests and ecumenicism. J. Hered. 1995, 86, 248–249. [Google Scholar] [CrossRef]
  29. Neumann, K.; Maak, S.; Stuermer, I.W.; von Lengerken, G.; Gattermann, R. Low microsatellite variation in laboratory gerbils. J. Hered. 2001, 92, 71–74. [Google Scholar] [CrossRef]
  30. Queller, D.C.; Goodnight, K.F. Estimating relatedness using genetic markers. Evolution 1989, 43, 258–275. [Google Scholar] [CrossRef]
  31. Peakall, R.; Smouse, P.E. GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 2006, 6, 288–295. [Google Scholar] [CrossRef]
  32. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2022; Available online: https://www.R-project.org/ (accessed on 31 July 2022).
  33. Wang, J. Marker-based estimates of relatedness and inbreeding coefficients: An assessment of current methods. J. Evol. Biol. 2014, 27, 518–530. [Google Scholar] [CrossRef]
  34. Taylor, H.R. The use and abuse of genetic marker-based estimates of relatedness and inbreeding. Ecol. Evol. 2015, 5, 3140–3150. [Google Scholar] [CrossRef]
  35. Robson, K.M.; Lamb, C.T.; Russello, M.A. Low genetic diversity, restricted dispersal, and elevation-specific patterns of population decline in American pikas in an atypical environment. J. Mammal. 2016, 97, 464–472. [Google Scholar] [CrossRef]
  36. Zgurski, J.M.; Hik, D.S. Gene flow and the restoration of genetic diversity in a fluctuating collared pika (Ochotona collaris) population. Conserv. Genet. 2014, 15, 37–48. [Google Scholar] [CrossRef]
  37. Zhou, L.; Yang, S.; Yu, Z.; Yin, B.; Huai, H.; Li, S.; Wei, W. Genetic diversity and differentiation in four natural populations of plateau pika (Ochotona curzoniae). Acta Theriol. Sin. 2007, 27, 221–228. [Google Scholar]
  38. Volodin, I.A.; Volodina, E.V.; Frey, R.; Karaseva, K.D.; Kirilyuk, V.E. Daurian pika (Ochotona dauurica) alarm calls: Individual acoustic variation in a lagomorph with audible through ultrasonic vocalizations. J. Mammal. 2021, 102, 947–959. [Google Scholar] [CrossRef]
  39. Quirici, V.; Faugeron, S.; Hayes, L.D.; Ebensperger, L.A. Absence of kin structure in a population of the group-living rodent Octodon degus. Behav. Ecol. 2011, 22, 248–254. [Google Scholar] [CrossRef]
  40. Lacey, E.A.; Wieczorek, J.R. Kinship in colonial tuco-tucos: Evidence from group composition and population structure. Behav. Ecol. 2004, 15, 988–996. [Google Scholar] [CrossRef]
  41. Zhu, X.D.; Li, X.J.; Du, X.Y.; Wang, Y.; Lu, J.; Chen, Z.W. Comparative analysis of population genetic structure for wild and domesticated Mongolian gerbils. Chin. J. Comp. Med. 2008, 18, 39–43. [Google Scholar]
  42. Liu, W.; Wang, G.; Wan, X.; Zhong, W. Winter food availability limits winter survival of Mongolian gerbils (Meriones unguiculatus). Acta Theriol. 2011, 56, 219–227. [Google Scholar] [CrossRef]
  43. Wang, G.; Liu, W.; Wang, Y.; Wan, X.; Zhong, W. Restricted dispersal determines fine-scale spatial genetic structure of Mongolian gerbils. Curr. Zool. 2017, 63, 687–691. [Google Scholar] [CrossRef]
  44. Wimmer, B.; Tautz, D.; Kappeler, P.M. The genetic population structure of the gray mouse lemur (Microcebus murinus), a basal primate from Madagascar. Behav. Ecol. Sociobiol. 2002, 52, 166–175. [Google Scholar] [CrossRef]
  45. Sumbh, O.; Hof, A.R. Can pikas hold the umbrella? Understanding the current and future umbrella potential of keystone species Pika (Ochotona spp.). Glob. Ecol. Conserv. 2022, 38, e02247. [Google Scholar] [CrossRef]
Diversity 14 00732 g001 550
Figure 1. Relationships between the genetic relatedness (Queller and Goodnight coefficients) and genetic diversity (Shannon diversity index) of (a) Daurian pikas and (b) Mongolian gerbils in Inner Mongolia, China. The letter β is the estimate of regression slope.
Figure 1. Relationships between the genetic relatedness (Queller and Goodnight coefficients) and genetic diversity (Shannon diversity index) of (a) Daurian pikas and (b) Mongolian gerbils in Inner Mongolia, China. The letter β is the estimate of regression slope.
Diversity 14 00732 g001
Diversity 14 00732 g002 550
Figure 2. Distributions of the Queller and Goodnight genetic relatedness coefficients for social groups of (a) Dauria pikas and (b) Mongolian gerbils in Inner Mongolia, China.
Figure 2. Distributions of the Queller and Goodnight genetic relatedness coefficients for social groups of (a) Dauria pikas and (b) Mongolian gerbils in Inner Mongolia, China.
Diversity 14 00732 g002
Table
Table 1. Summaries of allelic diversity and heterozygosity for 11 microsatellite markers cross-amplified in Daurian pika, Inner Mongolia, China.
Table 1. Summaries of allelic diversity and heterozygosity for 11 microsatellite markers cross-amplified in Daurian pika, Inner Mongolia, China.
occ2ocp1ocp2ocp3ocp5p7Fp47Fp124Rp149Fp156Fp172R
Number of alleles1067191726141931825
Number of effective alleles4.012.233.589.678.5214.4710.8710.1013.742.7810.69
Shannon diversity index1.661.001.502.492.352.862.492.482.911.432.68
Observed heterozygosity (Ho)0.680.580.490.680.800.500.820.790.680.420.84
Expected heterozygosity (He) 0.750.550.720.900.880.930.910.900.930.640.91
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Wang, G.; Wan, X.; Liu, W.; Shan, X. Genetic Diversity and Relatedness of Group-Living Small Mammals on the Mongolian Plateau. Diversity 2022, 14, 732. https://doi.org/10.3390/d14090732

AMA Style

Wang G, Wan X, Liu W, Shan X. Genetic Diversity and Relatedness of Group-Living Small Mammals on the Mongolian Plateau. Diversity. 2022; 14(9):732. https://doi.org/10.3390/d14090732

Chicago/Turabian Style

Wang, Guiming, Xinrong Wan, Wei Liu, and Xueyan Shan. 2022. "Genetic Diversity and Relatedness of Group-Living Small Mammals on the Mongolian Plateau" Diversity 14, no. 9: 732. https://doi.org/10.3390/d14090732

APA Style

Wang, G., Wan, X., Liu, W., & Shan, X. (2022). Genetic Diversity and Relatedness of Group-Living Small Mammals on the Mongolian Plateau. Diversity, 14(9), 732. https://doi.org/10.3390/d14090732

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop