Title:

Biased sex-ratio in woodland grouse population of the Tatra National Park, suggested by molecular sexing of non-invasive samples

Subtitle:

Biased sex-ratio in woodland grouse population of the Tatra NP ; Molekularna identyfikacja płci wykonana na podstawie nieinwazyjnych prób sugeruje zaburzoną proporcję płci w populacji głuszca i cietrzewia w Tatrzańskim Parku Narodowym

Creator:

Santorek, Anna ; Zwijacz-Kozica, Tomasz ; Dulisz, Beata ; Merta, Dorota ; Rutkowski, Robert (zootechnika)

Publisher:

Museum and Institute of Zoology Polish Academy of Sciences

Place of publishing:

Warszawa

Date issued/created:

2020

Description:

129-136 p.

Type of object:

Journal/Article

Subject and Keywords:

Tetrao urogallus ; Lyrurus tetrix ; sex ratio ; genetic sexing ; non-invasive sampling

Abstract:

Sex ratio (ratio between the number of male and female individuals in a population) is an important factor contributing to the survival rates of the population in wild. Imbalanced sex ratio is often the cause of diminished survival rates of endangered species. The analysis of DNA collected through noninvasive methodologies effectively allows to monitor populations of rare species or species that are difficult to observe in the wild. Such method was used to determine the sex ratio in populations of the capercaillie (Tetrao urogallus) and black grouse (Lyrurus tetrix) in the Tatra National Park. We collected over 250 samples (mostly excrement) in the area of the Tatra National Park and identified species via microsatellite genotyping and determined the sex using fragments of the CHD gene. We found that the majority of the samples belonged to male specimens irrespective of the species suggesting a large deviation from an equal sex ratio in wild populations of capercaillie and black grouse in the Tatra National Park. Our results point out the fundamental contribution of genetic assessment of sex ration to monitor the viability of both species in the Tatra National Park

References:

ALATALO R. V., HÖGLUND J., LUNDBERG A. & SUTHERLAND W. J. 1992. Evolution of black grouse leks: female preferences benefit males in larger leks. Behavioral Ecology 3 (1): 53–59. DOI: https://doi.org/10.1093/beheco/3.1.53
BAUMGARDT J. A., GOLDBERG C. S., REESE K. P., CONNELLY J. W., MUSIL D. D., GARTON E. O. & WAITS L. P. A. 2013. Method for estimating sex ratio for sage-grouse using noninvasive genetic samples. Molecular Ecology Resources 13:393–402. DOI: https://doi.org/10.1111/1755-0998.12069
BEJA-PEREIRA A., OLIVEIRA R., ALVES P.C., SCHWARTZ M. K. & LUIKART G. 2009. Advancing ecological understandings through technological transformations in noninvasive genetics. Molecular Ecology Resources 9: 1279–1301. DOI: 10.1111/j.1755-0998.2009.02699.x
BESSA-GOMES C. S., LEGENDRE S. & CLOBERT J. 2004. Allee effects, mating systems and the extinction risk in populations with two sexes. Ecology Letters 7: 802–812. DOI: https://doi.org/10.1111/j.1461-0248.2004.00632.x
BLACKMORE C. J., PEAKALL R. & HEINSOHN R. 2011. The absence of sex‐biased dispersal in the cooperatively breeding grey‐crowned babbler. Journal of Animal Ecology 80(1): 69–78. DOI: https://doi.org/10.1111/j.1365-2656.2010.01761.x
BONIN A., BELLEMAIN E., BRONKEN EIDESEN P., POMPANON F., BROCHMANN C. & TABERLET P. 2004. How to track and assess genotyping errors in population genetics studies. Molecular Ecology 13: 3261–3273. DOI: 10.1111/j.1365-294X.2004.02346.x
BRICKLE N. W., DUCKWORTH J. W., TORDOFF A. W., POOLE C. M., TIMMINS R. & MCGOWAN P. J. 2008. The status and conservation of Galliformes in Cambodia, Laos and Vietnam. Biodiversity and Conservation. 17(6): 1393–1427. DOI: 10.1007/s10531-008-9346-z
BROQUET T., & PETIT E. 2004. Quantifying genotyping errors in noninva-sive population genetics. Molecular Ecology 13:3601–3608. DOI: 10.1111/j.1365-294X.2004.02352.x
BROQUET T., MENARD N. & PETIT E. 2007. Noninvasive population genetics: a review of sample source, diet, fragment length and microsatellite motif effects on amplification success and genotyping error rates. Conservation Genetics 8: 249–260. DOI: 10.1007/s10592-006-9146-5
BUSH K. L., VINSKY M. D., ALDRIDGE C. L., & PASZKOWSKI C. A. 2005. A comparison of sample types varying in invasiveness for use in DNA sex determination in an endangered population of greater Sage-Grouse (Centrocercus uropihasianus). Conservation Genetics 6(5): 867–870. DOI: 10.1007/s10592-005-9040-6
CAIZERGUES A., DUBOIS S., MONDOR G. & RASPLUS J.F. 2001. Isolation and characterisation of microsatellite loci in black grouse (Tetrao tetrix). Molecular Ecology Notes 1 (1-2): 36–38. DOI: 10.1046/j.1471-8278.2000.00015.x
CAIZERGUES A., RÄTTI O., HELLE P., ROTELLI L., ELLISON L. & RASPLUS J. Y. 2003. Population genetic structure of male black grouse (Tetrao tetrix L.) in fragmented vs. continuous landscapes. Molecular Ecology. 12 (9): 2297–2305. DOI: 10.1046/j.1365-294x.2003.01903.x
CIACH M. 2016. Cietrzew Tetrao tetrix. Pp. 135–142. In: WILK T., BOBREK R., PĘPKOWSKA-KRÓL A., NEUBAUER G.,KOSICKI J. Z. (eds), Ptaki polskich Karpat – stan, zagrożenia, ochrona. OTOP: Marki, Poland.
CLOUT M. N., ELLIOTT G. P. & ROBERTSON B. C. 2002. Effects of supplementary feeding on the offspring sex ratio of kakapo: a dilemma for the conservation of apolygynous parrot. Biological Conservation 107: 13–18. DOI: 10.1016/S0006-3207(01)00267-1
CORRALES C. & HÖGLUND J. 2012. Maintenance of gene flow by female-biased dispersal of Black Grouse Tetrao tetrixin northern Sweden. Journal of Ornithology 153(4): 1127-1139. DOI: 10.1007/s10336-012-0844-0
CLUTTON-BROCK T. H. 1986. Sex ratio variation in birds. Ibis 128: 317–329. DOI: https://doi.org/10.1111/j.1474-919X.1986.tb02682.x
CLUTTON-BROCK T. H & VINCENT A. C. J. 1991. Sexual selection and the potential reproductive rates of males and females. Nature 351:58–60. DOI: 10.1038/351058a0
DONALD P. 2007. Adult sex ratios in wild bird populations. Ibis 149: 671–692. DOI: 10.1111/j.1474-919X.2007.00724.x
DUBIEC A. & ZAGALSKA-NEUBAUER M. 2006. Molecular techniques for sex identification in birds. Biological Letters. 43(1): 3-12.
DURÃES R., LOISELLE B. A., PARKER P. G. & BLAKE J. G. 2009. Female Mate Choice Across Spatial Scales: Influence of Lek and Male Attributes on Mating Success of Blue-Crowned Manakins. Proceedings of the Royal Society B: Biological Sciences 276 (1663): 1875–1881. DOI:10.1098/rspb.2008.1752
EGGERT L. S., EGGERT J. A. & WOODRUFF D. S. 2003. Estimating population sizes for elusive animals: the forest elephants of Kakum National Park, Ghana. Molecular ecology 12 (6): 1389–1402. DOI: 10.1046/j.1365-294X.2003.01822.x
ELLEGREN H. & SHELDON B. 1997. New tools for sex identification and the study of sex allocation in birds. Trends in Ecology & Evolution 12:255–259. DOI: 10.1016/s0169-5347(97)01061-6
ELLISON L. N. & MAGNANI Y. 1985. Eléments de dynamique de population du Tétras lyre (Tetrao tetrix) dans les Alpes Françaises. — Gibier Faune Sauvage. Game & Wildlife Science 2: 63–84.
FISHER R. 1930. Genetical theory of sex allocation. Clarendon Press. London
FONTANESI L., TAZZOLI M., PECCHIOLI E., HAUFFE H. C., ROBINSON T. J. & RUSSO V. 2008. Sexing European rabbits (Oryctolagus cuniculus), European brown hares (Lepus europaeus) and mountain hares (Lepus timidus) with ZFX and ZFY loci. Molecular Ecology Resources 8(6): 1294-1296. DOI: https://doi.org/10.1111/j.1755-0998.2008.02167.x
HARDY I. C. W. 2002. Sex Ratios: Concepts and Research Methods. Cambridge University Press. Cambridge.
HELLE P., KURKI S. & LINDEN H. 1999. Change in the sex ratio of the Finnish capercaillie Tetrao urogallus population. Wildlife Biology 5: 25–31. DOI: https://doi.org/10.2981/wlb.1999.005
HORI T., ASAKAWA S., ITOH Y., SHIMIZU N. &MIZUNO S. 2000. WPKCI, encoding an altered form of PKCI, is conserved widely on the avian W chromosome and expressed in early female embryos. Molecular Biology of the Cell 11:3645–3660. DOI: 10.1091/mbc.11.10.3645
HÖRNFELDT B., HIPKISS T. & EKLUND U. 2001. Juvenile sex ratio in relation to breeding success in capercaillie Tetrao urogallus and black grouse T. tetrix. Ibis 143: 627-631. DOI: 10.1111/j.1474-919X.2001.tb04890.x
JOHNSON P. C. & HAYDON D. T. 2007. Maximum-likelihood estimation of allelic dropout and false allele error rates from microsatellite genotypes in the absence of reference data. Genetics 175 (2): 827–842. DOI: 10.1534/genetics.106.064618
KIDWAI Z., SANKAR K., QUERSHI Q. & KHAN J. A. 2011. Abundance and habitat utilisation by Galliformes in the Sariska Tiger Reserve, Rajasthan, India. International Journal of Galliformes Conservation 2: 54-60.
LAMBERTUCCI S. A., CARRETE M., SPEZIALE K. L., HIRALDO F. & DONÁZAR J. A. 2013. Population sex ratios: another consideration in the reintroduction–reinforcement debate? PloS One 8: e75821. DOI: 10.1371/journal.pone.0075821
LEE A. M., SÆTHER B.-E. & ENGEN S. 2011. Demographic Stochasticity, Allee Effects, and Extinction: The Influenceof Mating System and Sex Ratio. The American Naturalist 177(3): 301–313. DOI: 10.1086/658344
LINDÉN H. 1981. Estimation of juvenile mortality in capercaillie Tetrao urogallus and the black grouse, Tetrao tetrixfrom indirect evidence. Finnish Game Research 39: 35-51.
LINDSTRÖM J., RINTAMÄKI P.T. & STORCH I. 1998. Black grouse—BWP update. The journal of birds of the Western Palearctic. Oxford University Press, Oxford 2:173–191.
MARTIC., BOSSERT A. &PAULI H. R .2016. Population trend of Black Grouse Tetrao tetrix and Rock Ptarmigan Lagopus muta in the Aletsch region (central Alps, Switzerland) from 1970 to 2015. Der Ornithologische Beobachter 113: 1 – 30.
MERTA D., KOBIELSKI J., KRZYWINSKI A. & RZOŃCA Z. 2013. Czynna ochrona głuszca Tetrao urogallus na terenie Borów Dolnośląskich. Studia i Materiały Centrum Edukacji Przyrodniczo-Leśnej 15: 195-209.
MORRISON C. A., ROBINSON R. A., CLARK J. A. & GILL J. A. 2016. Causes and consequences of spatial variation in sex ratios in a declining bird species. Journal of Animal Ecology 85: 1298-1306. DOI: 10.1111/1365-2656.12556
MOSS R. & OSWALD J. 1985. Population dynamics of Capercaillie in a North-east Scottish glen. Ornis Scandinavica 16(3): 229-238. DOI: 10.2307/3676635
MOSS R., PICOZZI N., SUMMERS R. W. & BAINES D. 2008. Capercaillie Tetrao urogallus in Scotland - demography of a declining population. Ibis 142(2): 259–267. DOI: 10.1111/j.1474-919X.2000.tb04865.x
NAVARA K. J. 2018a. Introduction to Vertebrate Sex Ratio Adjustment. In: Choosing Sexes. Fascinating Life Sciences. Cham, Switzerland: Springer.
NAVARA K. J. 2018b. The Bees Do It, but What About the Birds? Evidence for Sex Ratio Adjustment in Birds. In: Choosing Sexes. Fascinating Life Sciences. Cham, Switzerland: Springer.
PEAKALL R. & SMOUSE P. E. 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics Applications Note 28: 2537–2539.
PÉREZ T., VÁZQUEZ J. F., QUIRÓS F. & DOMÍNGUEZ A. 2011. Improving non-invasive genotyping in capercaillie (Tetrao urogallus): redesigning sexing and microsatellite primers to increase efficiency on faeces samples. Conservation Genetics Resources 3(3): 483-487. DOI: 10.1007/s12686-011-9385-8
PIERTNEY S. B.&HÖGLUND J. 2001. Polymorphic microsatellite DNA markers in black grouse (Tetrao tetrix). Molecular Ecology Notes 1(4): 303–304. DOI: 10.1046/j.1471-8278
PIGGOTT M. P., BELLEMAIN E., TABERLET P. & TAYLOR A.C. 2004. A multiplex pre-amplification method that significantly improves microsatellite amplification and error rates for faecal DNA in limiting conditions. Conservation Genetics 5(3): 417-420. DOI: 10.1023/B:COGE.0000031138.67958.44
PRYKE S. R. & ROLLINS L.A. 2012. Mothers adjust offspring sex to match the quality of the rearing environment. Proceedings of the Royal Society B: Biological Sciences 279(1744): 4051-7. DOI: 10.1098/rspb.2012.1351
REGNAUT S., LUCAS F. S. & FUMAGALLI L. 2006. DNA degradation in avian faecal samples and feasibility of noninvasive genetic studies of threatened capercaillie populations. Conservation Genetics 7 (3): 449–453. DOI: 10.1007/s10592-005-9023-7
ROBERTSON B. C., ELLIOTT G. P., EASON D. K., CLOUT M. N. & GEMMELL N. J. 2006. Sex allocation theory aids species conservation. Biology Letters 2(2): 229–231. DOI: 10.1098/rsbl.2005.0430
RUTKOWSKI R., SUCHECKA E. & ZAWADZKA D. 2013. Migracyjność zależna od płci a genetyczna struktura populacji kuraków leśnych. Postępy Techniki w Leśnictwie. 122: 28–33
RUTKOWSKIR., DULISZ B., SZCZEPAŃSKI S., NOWAKOWSKIJ.J., ZWIJACZ−KOZICA T. & KRZAN P. 2017a. Conservation genetics of the capercaillie in Poland – estimating the size of the Tatra National Park population by the genotyping of non−invasive samples. Fragmenta Faunistica 60(2): 119−128. DOI: 10.3161/00159301FF2017.60.2.119
RUTKOWSKI R., ZAWADZKA D., SUCHECKA E. & MERTA D. 2017b. Conservation genetics of the capercaillie in PolandDelineation of conservation units. PLoS One 12(4): p.e0174901. DOI: 1
SANTOREK A., KULIGOWSKA B., SZCZEPAŃSKI S., DULISZ B. & RUTKOWSKI R. 2018. Ocena liczebności głuszca (Tetrao urogallus) w Babiogórskim Parku Narodowym na podstawie analiz genetycznych prób nieinwazyjnych. Studia i Materiały Centrum Edukacji Przyrodniczo-Leśnej w Rogowie 54 (4): 125−133.
SEGELBACHER G., PAXTON R.J., STEINBRUCK G., TRONTELJ P. & STORCH I. 2000. Characterization of microsatellites in capercaillie Tetrao urogallus (Aves). Molecular Ecology 9(11): 1934–1935. DOI: 10.1046/j.1365-294x.2000.0090111934.x
SEGELBACHER G. & STEINBRÜCK G. 2001. Bird faeces for sex identification and microsatellite analysis. Vogelwarte 41:139-142
SEGELBACHER G., MANEL S. & TOMIUK J. 2008. Temporal and spatial analyses disclose consequences of habitat fragmentation on the genetic diversity in capercaillie (Tetrao urogallus). Molecular Ecology 17 (10): 2356–2367. DOI: 10.1111/j.1365-294X.2008.03767.x
STORCH I. 1995. Annual home ranges and spacing patterns of capercaillie in central Europe. The Journal of Wildlife Management 59: 392–400. DOI: https://doi.org/10.2307/3808953
STORCH I. & SEGELBACHER G. 2000. Genetic correlates of spatial population structure in central European capercaillie Tetrao urogallus and black grouse T. tetrix: a project in progress. Wildlife Biology 6:305–310. DOI: 10.2981/wlb.2000.014
STORCH I. (ed.). 2007. Grouse – Status Survey and Action Plan 2006–2010. IUCN. Gland Switzerland and Cambridge UK and World Pheasant Association, Fordinbridge, UK.
SUN Y. H., SWENSON J. E., FANG Y., KLAUS S. & SCHERZINGER W. 2003. Population ecology of the Chinese grouse, Bonasa sewerzowi, in a fragmented landscape. Biological Conservation 110 (2): 177–184. DOI: 10.1016/S0006-3207(02)00187-8
TABERLET P., WAITS L. P. & LUIKART G. 1999. Noninvasive genetic sampling: look before you leap. Trends in Ecology & Evolution 14: 323–327. DOI: 10.1016/s0169-5347(99)01637-7
THÉRY M. 1992. The evolution of leks through female choice: differential clustering and space utilization in six sympatric manakins. Behavioral Ecology and Sociobiology 30 (3): 227–237. DOI: 10.1007/BF00166707
TRIVERS R. L. & WILLARD D. E. 1973. Natural Selection of Parental Ability to Vary the Sex Ratio of Offspring. Science 179(4068): 90–92. DOI: 10.1126/science.179.4068.90
VANDERKIST B. A., XUE X. H., GRIFFITHS R., MARTIN K., BEAUCHAMP W. & WILLIAMS T. D. 1999. Evidence of male‐bias in capture samples of Marbled Murrelets from genetic studies in British Columbia. The Condor 101: 398–402. DOI: https://doi.org/10.2307/1370004
WAITS L.P. & PAETKAU D. 2005. Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. Journal of Wildlife Management 69(4): 1419-1433. DOI: 10.2193/0022-541X(2005)69[1419:NGSTFW]2.0.CO;2
WEST S.A. 2002. Constraints in the Evolution of Sex Ratio Adjustment. Science 295 (5560): 1685–1688. DOI: 10.1126/science.1069043
WEST S. 2009. Sex Allocation. Princeton University Press. Princeton. NJ.
WILKINSON N. I., EATON M. A., MARSHALL G. & HAYSOM S. 2018. The population status of Capercaillie Tetrao urogallus in Scotland during winter 2015–16. Bird Study 65(1): 1-16. DOI: 10.1080/00063657.2018.1439448
YAMASHIRO A., KANESHIRO Y., KAWAGUCHI Y. & YAMASHIRO T. 2017. Species, sex, and individual identification of Japanese serow (Capricornis crispus) and sika deer (Cervus nippon) in sympatric region based on the fecal DNA samples. Conservation Genetics Resources 9(2): 333–338. DOI: 10.1007/s12686-016-0665-1
ZBINDEN N., SALVIONI M., KORNER-NIEVERGELT F. & KELLER V. 2018. Evidence for an additive effect of hunting mortality in an alpine black grouse Lyrurus tetrix population. Wildlife Biology 2018(1): wlb.00418. DOI: 10.2981/wlb.00418.

Relation:

Fragmenta Faunistica

Volume:

63

Issue:

2

Start page:

129

End page:

136

Resource type:

Text

Detailed Resource Type:

Article

Resource Identifier:

10.3161/00159301FF2020.63.2.129

Source:

MiIZ PAN, call no. P.256 ; MiIZ PAN, call no. P.4664 ; click here to follow the link

Language:

eng ; eng

Rights:

Creative Commons Attribution BY 3.0 PL license

Terms of use:

Copyright-protected material. [CC BY 3.0 PL] May be used within the scope specified in Creative Commons Attribution BY 3.0 PL license, full text available at: ; -

Digitizing institution:

Museum and Institute of Zoology of the Polish Academy of Sciences

Original in:

Library of the Museum and Institute of Zoology PAS

Access:

Open