Genus Bison has the Biggest Sex-Related Difference in Longevity among Mammals

The genus Bison is a representative of large even-toed ungulates. The first members appeared at the beginning of the Pleistocene in India and China. Bison has later spread from Asia to Europe and America. Archaeological evidence shows that two bison species, the steppe bison (B. priscus) and the woodland bison (B. schoetensacki), existed in Europe from the Middle Pleistocene. Only two bison species have survived until today: American bison (B. bison) and European bison (B. bonasus), known also as a wisent. It was assumed, that these closely related species are derived from the extinct long-horned steppe bison. However, a recent study has found out that the woodland bison is a sister species of European bison, which excludes the steppe bison being a direct ancestor of European bison [1].

The European bison genome reflects a common descent, where the nuclear genome is closely related to that of American bison [2- 4], in agreement with morphological evidence and the fact that the two bison species can produce completely fertile hybrid offspring. On the other hand, the mitochondrial genome of European bison is similar to aurochs (Bos primigenius) and cattle (Bos taurus) genome rather than to the American bison genome [2,5,6]. In general, several morphological and behavioural traits, which distinguished European bison from its American relative, have been found. Adult individuals of European bison have smaller body length, less body hair [7] and are mixed feeders combining browsing and grazing [8-10], whereas American bison is primarily grazer [11].

European bison went through a severe population bottleneck and became extinct in the wild at the beginning of 20th century. The descendants of just 12 animals out of the 54 remaining European bison living in captivity at the beginning of the 1920s were involved in species restoration. Two genetic lines of European bison has been diversified: the lowland line (L), and the hybrid lowland-Caucasian line (LC) [12]. The lowland line of European bison originates from only seven founders. Approximately 80% of the genes in the contemporary population come from just two founders. The average inbreeding level in the L line of European bison is almost 50% and 28% in the LC line [12].

In North America, American bison includes two subspecies: the plains bison (B. bison bison) and the wood bison (B. bison athabascae). Similarly, as European bison, American bison went through a population bottleneck too. The plains bison has been saved from extinction, especially thanks to ranchers. However, today’s population of plains bison comes from less than 100 founders [13].

Once almost wiped out from existence, the mighty bison has recovered to become a symbol of pride for the Americ and European conservation efforts. Both species have been extensively studied from the evolutionary [1,14,15], genetic [16- 19], behavioural [8,20] and conservation [21,22] point of view. Interestingly, only limited and statistically not evaluated data of longevity has been presented in bison species until today. European bison is estimated to live up to 27 years in the wild [23] and up to 28 years [24,25] in captivity. American bison is estimated to live up to 25 years in the wild [23] with a record of more than 33.5 years old individual living in captivity [24]. The objective of this study is to describe the longevity of European (L and LC line) and American bison using the statistically significant data and to compare the sexrelated differences in the longevity.

Materials and Methods

Data of 1206 deceased European bison were obtained from the European Bison Pedigree Book (www.bpn.com.pl). Recorded data were the line, sex, date of birth and date of death. Data of 2912 deceased American bison were obtained from the information system for zoological gardens ZIMS (www.species360.org). Recorded data were sex, date of birth and date of death. Lifespans specific for European bison (L and LC line) and for American bison were reported using median. Median lifespan of both lines of European bison, American bison and sex-related differences in lifespan were compared using Mann-Whitney U test [26].

For the first time, we described the median lifespan of European bison and American bison. Median lifespan was determined to 3.54 years in European bison and to 3.31 years in American bison. Median lifespan of the European bison L and LC line was determined to 3.58 years and 3.51 years, respectively. Data are summarized in Table 1. Median lifespan of the European bison L line and the European bison LC line did not differ statistically using Mann-Whitney U test (p=0.7667). These data confirmed that no difference in the longevity exists between L and LC line of European bison. However, the median lifespan was lower than expected. Low median lifespan is influenced by high mortality of young animals under the age of four years inspite of the fact that very high mortality of young animals is rare in mammals. Moreover, we found highly significant differences in the longevity between the sex in European bison as well as in American bison. Median lifespan of female European bison (6.01 years) exceeded more than two times median lifespan of male (2.71 years), see Table 1 and Figure 1. The difference between both sexes was statistically proved (p< 0.001). Similar differences in sex-related lifespan were found in L and LC line of European bison Table 1.

Table 1:Median lifespan of american and european bison.

Abbreviations:A. bison: American Bison; E. bison: European Bison; n: Number of Animals; M: Male; F: Female; L: Lowland line; LC: Lowland-Caucasian line.

Figure 1:Median lifespan of European bison and American bison. E. bison: European Bison; A. bison: American Bison.

Median lifespan of female American bison (6.64 years) exceeded more than three times median lifespan of male (2.12 years), see Table 1 and Figure 1. The difference between both sexes was statistically proved (p< 0.001). The reason for the biggest difference connected to sex in American and European bison among mammals is associated with the facts that mortality of young European bison males under the age of four years is substantially higher than mortality of young females of the same age and, similarly, mortality of young American bison males under the age of two years is substantially higher than mortality of young females of the same age. Among mammals, a difference like this has not been described yet. Generally, in most mammalian species including human, females live longer than males [27,28]. The biggest known difference in longevity between sexes among mammals has been described in short-finned pilot whale, where females live nearly twice as long as males [29], whereas only a small effect of sex was observed on canine longevity [30] and no sex-related difference in the longevity was found in Cane Corso dogs [31].

In our study, mortality of European bison (L and LC line) and American bison at the different age was evaluated. Results are summarized in Figure 2. Mortality of young European bison males (L and LC line) under the age of four years was higher than mortality of young females of the same age Figure 2A, 2B & 2C. Similarly, mortality of young American bison males under the age of two years was higher than mortality of young females of the same age Figure 2D. The cause of higher young male mortality could be linked to high inbreeding level. In the European bison L line, inbreeding level is almost 50%, whereas in the European bison LC line the level is 28% [12]. It is not clear if high inbreeding levels negatively influenced mortality of young males because inbreeding level of American bison is probably much lower than inbreeding level of European bison, but the mortality of young males of American bison is also very high. This is going to be the main topic of our further research.

Figure 2:Percentage of mortality at different age. A. bison: American Bison; E. bison: European Bison; L: Lowland line; LC: Lowland-Caucasian line.

The median lifespan of European and American bison was determined for the first time. The median lifespan of female European bison exceeded more than two times the median lifespan of male. Similar finding was found in American bison, where the median lifespan of female exceeded more than three times the median lifespan of male. These differences in the longevities represent the biggest sex-related differences in the longevity among mammals. The reason of the difference is associated with the facts that mortality of young American bison males as well as European bison males is significantly higher than mortality of young females. A detailed study of these differences using methods of molecular genetics may help to clarify the genetic factors linked to longevity.

We wish to thank Jan Raczyński and Malgorzata Bolbot (Editorial Office of European bison Pedigree Book, Poland) for valuable advice. We also thank following colleagues and institutions for cooperation: Bellewaerde Park (Wesley Parmentier, Belgium); Česká krajina (Dalibor Dostál, Czech Republic); Podilskyj zoopark VOKSPL (Juliya Ivashuk, Ukraine); Podkrušnohorský zoopark Chomutov (Jan Mengr, Czech Republic), Tierpark Bern (Marc Rosset, Switzerland); Vojenské lesy a statky ČR (Miloslav Zikmund, Czech Republic); Western Pomeranian Natural Society (Marcin Grzegorzek, Poland); Wildpark Lüneburger Heide Tietz KG (Alexandra Urban, Germany); ZOO Kiev (Yegor Yakovlev, Ukraine); ZOO Olomouc (Jitka Vokurková, Czech Republic); ZooBotánico de Jerez (Mariano Cuadrado Gutierrez, Spain) and Zoological Society of London (Lewis Rowden, United Kingdom).

1. Palacio P, Berthonaud V, Guérin C, Lambourdière J, Maksud F et al. (2017) Genome data on the extinct bison schoetensacki establish it as a sister species of the extant European bison (Bison bonasus). BMC Evol Biol 17: 48.
2. Verkaar EL, Nijman IJ, Beeke M, Hanekamp E, Lenstra JA (2004) Maternal and paternal lineages in cross-breeding bovine species. Has wisent a hybrid origin? Mol Biol Evol 21(7): 1165-1170.
3. Nijman IJ, Boxtel VDCJ, Cann VLM, Marnoch Y, Cuppen E, et al. (2008) Phylogeny of Y chromosomes from bovine species. Cladistics 24(5): 723- 726.
4. Hassanin A, An J, Ropiquet A, Nguyen TT, Couloux A (2013) Combining multiple autosomal introns for studying shallow phylogeny and taxonomy of laurasiatherian mammals: Application to the tribe bovini (Cetartiodactyla, Bovidae). Mol Phylogenet Evol 66(3): 766-775.
5. Zeyland J, Wolko L, Lipiński D, Woźniak A, Nowak A, et al. (2012) Tracking of wisent-bison-yak mitochondrial evolution. J Appl Genet 53(3): 317-322.
6. Hassanin A, Delsuc F, Ropiquet A, Hammer C, Vuuren JVB, et al. (2012) Pattern and timing of diversification of cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. C R Biol 335(1): 32-50.
7. Krasińska M, Krasiński ZA (2002) Body mass and measurements of the European bison during postnatal development. Acta Theriologica 47(1): 85-106.
8. Gebczyńska Z, Gebczyński M, Martynowicz E (1991) Food eaten by freeliving European bison in białowieża forest. Acta Theriologica 36(3-4): 307-313.
9. Kowalczyk R, Taberlet P, Coissac E, Valentini A, Miquel C, et al. (2011) Influence of management practices on large herbivore diet-Case of European bison in bialowieza primeval forest (Poland). Forest Ecology and Management 261(4): 821-828.
10. Merceron G, Kaminska HE, Kowalczyk R (2014) 3D dental microwear texture analysis of feeding habits of sympatric ruminants in the bialowieza primeval forest, Poland. Forest Ecology and Management 328: 262-269.
11. Bergmann GT, Craine JM, Robeson MS, Fierer N (2011) Seasonal shifts in diet and gut microbiota of the American bison (Bison bison). PloS one 10(11): e0142409.
12. Tokarska M, Pertoldi C, Kowalczyk R, Perzanowski K (2011) Genetic status of the European bison Bison bonasus after extinction in the wild and subsequent recovery. Mammal Review 41(2): 151-162.
13. Hedrick PW (2009) Conservation genetics and north american bison (Bison bison). J Hered 100(4): 411-420.
14. Gautier M, Goudarzi MK, Levéziel H, Parinello H, Grohs C, et al. (2016) Deciphering the wisent demographic and adaptive histories from individual whole genome sequences. Mol Biol Evol 33(11): 2801-2814.
15. Froese D, Stiller M, Heintzman PD, Reyes AV, Zazula GD, et al. (2017) Fossil and genomic evidence constrains the timing of bison arrival in north america. Proc Natl Acad Sci USA 114(13): 3457-3462.
16. Gralak B, Krasińska M, Niemczewski C, Krasiński ZA, Zurkowski M (2004) Polymorphism of bovine microsatellite DNA sequences in the lowland European bison. Acta Theriologica 49(4): 449-456.
17. Tokarska M, Kawalko A, Wojcik JM, Pertoldi C (2009) Genetic variability in the European bison (Bison bonasus) population from bialowieza forest over fifty years. Biological Journal of the Linnean Society 97(4): 801-809.
18. Tokarska M, Marshall T, Kowalczyk R, Wójcik JM, Pertoldi C, et al. (2009) Effectiveness of microsatellite and SNP markers for parentage and identity analysis in species with low genetic diversity: the case of European bison. Heredity 103(4): 326-332.
19. Pertoldi C, Tokarska M, Wójcik JM, Demontis D, Loeschcke V, et al. (2009) Depauperate genetic variability detected in the american and European bison using genomic techniques. Biol Direct 4(1): 48.
20. Lott DF (1991) American bison socioecology. Applied Animal Behaviour Science 29(1-4): 135-145.
21. Olech W (2008) Bison bonasus. The IUCN Red List of Threatened Species. IUCN.
22. Gates CC, Freese CH, Gogan PJP, Kotzman M (2010) American bison: Status Survey and Conservation Guidelines. IUCN.
23. Grzimek B (1990) Grzimek’s encyclopedia of mammals. McGraw-Hill Publishing Company, New York, USA.
24. Weigl R (2005) Longevity of mammals in captivity; from the living collections of the world. Schweizerbart Science Publishers, Stuttgart, Germany.
25. Pucek Z, Belousova IP, Krasińska M, Krasiński ZA, Olech W (2002) European bison (Bison Bonasus): current state of the species and an action plan for its conservation. Mammal Research Institute, Polish Academy of Sciences, South Africa.
26. Mann HB, Whitney DR (1947) On a test of whether one of two random variables is stsochastically larger than the other. Ann Math Statist 18(1): 50-60.
27. Bronikowski AM, Altmann J, Brockman DK, Cords M, Fedigan LM, et al. (2011) Aging in the natural world: comparative data reveal similar mortality patterns across primates. Science 331(6022): 1325-1328.
28. Austad SN, Fischer KE (2016) Sex differences in lifespan. Cell Metab 23(6): 1022-1033.
29. Kasuya T, Marsh H (1984) Life history and reproductive biology of the short-finned pilot whale, globicephala macrorhynchus, off the pacific coast of japan. Rep Int Whal Commn 6: 259-310.
30. Hoffman JM, O’Neill DG, Creevy KE, Austad SN (2018) Do female dogs age differently than male dogs? The Journals of Gerontology: Series A 73(2): 150-156.
31. Korec E, Chalupa O, Hančl M, Korcová J, Bydžovská M (2017) Longevity of cane corso italiano dog breed and its relationship with hair colour. Open Vet J 7(2): 170-173.