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Genetic Evidence for Multiple Paternity in the Critically Endangered Cuban Crocodile (Crocodylus Rhombifer)

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Genetic Evidence for Multiple Paternity in the Critically Endangered Cuban Crocodile (Crocodylus Rhombifer) Amphibia-Reptilia (2016) DOI:10.1163/15685381-00003056 Genetic evidence for multiple paternity in the critically endangered Cuban crocodile (Crocodylus rhombifer) Yoamel Milián-García1,2,3,*, Evelyn L. Jensen2, Sheila Ribalta Mena1, Etiam Pérez Fleitas4, Gustavo Sosa Rodríguez4, Leiter Guerra Manchena4, Georgina Espinosa López1, Michael A. Russello2,* Abstract. Conservation strategies can be most effective when factors influencing the persistence of populations are well- understood, including aspects of reproductive biology such as mating system. Crocodylians have been traditionally associated with a polygynous mating system, with genetic studies revealing multiple paternity of clutches in several species. The endemic Cuban crocodile, Crocodylus rhombifer, is currently listed as Critically Endangered, and is one of the least understood crocodylian species in terms of its mating behavior. Here, we tested a hypothesis of multiple paternity in the Cuban crocodile by collecting genotypic data at nine microsatellite loci for 102 hatchlings from five nests sampled at the Zapata Swamp captive breeding facility and analyzing them in relation to data previously collected for 137 putative parents. All five nests showed evidence of multiple paternity based on the numbers of alleles per locus, with sibship analyses reconstructing all nests as having four to six full-sib family groups. Accordingly, mean pairwise relatedness values per nest ranged from 0.21 to 0.39, largely intermediate between theoretical expected values for half-siblings (0.25) and full-siblings (0.50). It is not possible to differentiate whether the multiple paternity of a nest was due to multiple matings during the same breeding season, or a result of sperm storage. Our results reveal that the C. rhombifer mating system is likely best characterized as promiscuous and suggest that the standard practice of enforcing a 1:2 sex ratio at the captive breeding facility should be altered in order to better maintain a demographically and genetically healthy ex situ population. Keywords: conservation genetics, mating system, polygamy, polygyny, promiscuity. Introduction mates sought, the presence and characteristics of pair bonding, and the patterns of parental A thorough understanding of factors that can in- care provided by each sex (Emlen and Oring, fluence the persistence of populations, includ- ing reproductive biology and mating system, 1977). Mating systems in animals can generally is important for setting conservation priorities be classified into three general types including: and implementing effective management plans 1) monogamy; 2) polygamy including polygyny (Dudash and Murren, 2008). The mating sys- (male mates with >1 female) and polyandry (fe- tem of a species encompasses the behavioral male mates with >1 male); and 3) promiscuity strategies used to obtain mates, the number of where both males and females mate with mul- tiple individuals (Emlen and Oring, 1977; Nun- ney, 1993). The species of the order Crocodylia 1 - Facultad de Biología, Universidad de La Habana, calle 25 # 455, e/J e I, Plaza Vedado, 10400 La Habana, Cuba have been traditionally associated with a polyg- 2 - Department of Biology, University of British Columbia, ynous mating system, with dominant males es- Okanagan Campus, 3333 University Way, Kelowna, V1V 1V7, British Columbia, Canada tablishing breeding territories, while excluding 3 - Centro de Investigaciones Marinas, Universidad de La other males and mating with multiple females ra ra Habana, calle 16 #114, e/1 y3 , Miramar, Playa, (Grigg and Kirshner, 2015). Yet, genetic studies 11300 La Habana, Cuba 4 - Empresa Nacional para la Protección de la Flora y la have revealed multiple paternity of clutches of Fauna, calle 42 y 514 Esq.7 Ave, Miramar, La Habana, eggs in several species across four of the nine Cuba genera within Crocodylia, including Alligator *Corresponding authors; e-mails to: [email protected], [email protected]; (Davis et al., 2001; Lance et al., 2009; Hu and [email protected] Wu, 2010), Caiman (Amavet et al., 2008, 2012; © Koninklijke Brill NV, Leiden, 2016. DOI:10.1163/15685381-00003056 2 Y. Milián-García et al. Oliveira et al., 2014), and Melanosuchus (Mu- eggs have been observed (Ramos Targarona, niz et al., 2011). The remaining genus, Crocody- 2013). Moreover, the wild C. rhombifer popu- lus, contains 12 of the 24 extant crocodylian lation is impacted by hybridization with the species, but the mating system of only four (C. widespread American crocodile (Crocodylus acutus, Budd et al., 2015; C. porosus,Lewiset acutus, Milian-Garcia et al., 2015). It is difficult al., 2013; C. moreletii, McVay et al., 2008; and to differentiate hybrids from non-hybrids in the C. intermedius, Rossi Lafferriere et al., 2016) wild based solely on morphological characters, has been evaluated using molecular markers. further complicating the study of reproductive The endemic Cuban crocodile, Crocodylus behavior based on simple observation. rhombifer, is currently listed as Critically En- An ex situ population of C. rhombifer is dangered (IUCN 2015), and is one of the least housed at the Zapata Swamp captive breed- understood crocodylians in terms of its repro- ing facility, but certain aspects of reproduc- ductive biology (Ramos Targarona, 2013). To tive strategy continue to be difficult to elu- study any aspect of the mating system of C. cidate. For example, this species copulates in rhombifer in the wild presents serious chal- the water, making the verification of success- lenges. The range of the species is limited ful mating attempts by direct observation dif- to a small area in Zapata Swamp (core zone ficult (fig. 1; online supplementary video 1). of 300 km2) that is extremely challenging to Harems are formed each reproductive season, access, and population sizes are severely re- but it is uncertain how many females are effec- duced due to illegal hunting and habitat degra- tively mated with the dominant male, or how dation (Milian-Garcia et al., 2011, 2015). Con- many times the male mates with each female sequently, direct observations of C. rhombifer (Ramos Targarona, 2013). There is also the pos- reproductive strategy in the wild are scarce. In sibility of “sneaker” males that may surrepti- over 37 years of monitoring the wild popu- tiously mate inside the harem of a dominant lation in Zapata Swamp, only 8 nests with male. Additionally, some females may move Figure 1. A pair of Cuban crocodiles mating within the breeding pen (C22) at the Zapata Swamp captive breeding facility. Images by YMG. This figure is published in colour in the online version. Genetic evidence for multiple paternity in the critically endangered Cuban crocodile (Crocodylus rhombifer) 3 among harems within a breeding season (Ramos a semi-closure of irregular shape (0.6 hectares) containing Targarona, 2013). marshy areas with free movement of water. Areas in which the animals are kept are subject to natural cyclical varia- The conservation of Crocodylus species that tions of drought and flood, similar to that taking place in inhabit Cuba is limited by this lack of knowl- the wild. The C22 breeding pen was founded in 1980 with edge of their basic biology and reproductive be- 100 females and 50 males from a selection of the first gen- eration offspring produced by the founders at the captive havior (Ramos Targarona, 2013; Alonso-Tabet breeding facility. The area of the pen that is not flooded is et al., 2014). In order to begin to fill this knowl- composed of peat mixed with river sand and covered with vegetation to allow nesting, equivalent to that which occurs edge gap, we tested the hypothesis of multiple in the wild. This breeding pen also includes different trees to paternity in the Cuban crocodile using geno- provide areas of shade and sunlight, enabling the animals to typic data collected for hatchlings and putative alternate spaces for optimal thermoregulation (Ramos Tar- garona, 2013). Males and females remain in this area for parents sampled from multiple nests in the Zap- exhibition and reproduction purposes, with a male-female ata Swamp ex situ population. We further dis- ratio of 1:2 and maintaining a total adult population size of cuss the importance of understanding the C. 150 (Ramos Targarona, 2013). Hatchlings (n = 102) were sampled from five nests lo- rhombifer mating system for informing in situ cated in the primary breeding pen (C22) during eclosion and ex situ conservation strategies. time in August 2010. All eggs were removed from each nest (online supplementary fig. S1) and transported to the incubation room available on-site at the facility. Each clutch was incubated separately in boxes made up of foam con- Materials and methods taining the same substrate available where the nests were built. This incubation strategy ensured no mixing of clutches Sampling prior to sampling. Samples consisted of a caudal scale from each hatchling’s tail, which is also used as a unique iden- This study took place at the Zapata Swamp captive breed- tifier to monitor the nests. All sampling was conducted ei- ing facility in Cuba (N 22°22.100 W 81°09.965 ; fig. 2, ta- ther directly by or under the supervision of the head vet- ble 1). This facility is run by the National Enterprise for erinarian of the facility (GSR). Each sample was preserved the Protection of Flora and Fauna in Cuba, the agency in in 95% ethanol until DNA extraction. All hatchlings were charge of approving all projects involving wildlife within classified as C. rhombifer based on external morphological the country. The primary reproductive pen, C22, constitutes characters and type of nest (mound) constructed by the fe- Figure 2. Map of Cuba with inset of Central America; the circle indicates the location of the Zapata Swamp captive breeding facility. Table 1. Sample size (N = number of hatchlings), mean Queller and Goodnight relatedness (RQG) and associated variance in parentheses, mean number of alleles (Na), mean observed (Ho) and expected heterozygosity (He) for each nest from the ex situ population of Crocodylus rhombifer in Zapata Swamp.
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