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Cryopreservation of Sperm Bundles (Spermatozeugmata) from Endangered T Livebearing Goodeids

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Cryopreservation of Sperm Bundles (Spermatozeugmata) from Endangered T Livebearing Goodeids Cryobiology 82 (2018) 49–56 Contents lists available at ScienceDirect Cryobiology journal homepage: www.elsevier.com/locate/cryo Cryopreservation of sperm bundles (spermatozeugmata) from endangered T livebearing goodeids ∗ Yue Liu, Leticia Torres, Terrence R. Tiersch Aquatic Germplasm and Genetic Resources Center, School of Renewable Natural Resources, Louisiana State University Agricultural Center, Baton Rouge, LA, USA ARTICLE INFO ABSTRACT Keywords: More than half of fishes in the family Goodeidae are considered to be endangered, threatened, or vulnerable. Cryopreservation Sperm cryopreservation is an effective tool for conserving genetic resources of imperiled populations, but de- Sperm velopment of protocols with livebearing fishes faces numerous challenges including the natural packaging of Sperm bundles sperm into bundles. In this study the cryopreservation of sperm bundles (spermatozeugmata) of three goodeids Spermatozeugmata species was evaluated. Sperm quality was evaluated by activation with NaCl-NaOH solution (at 300 mOsmol/kg Livebearing fish and pH 11.8), and analysis of dissociable bundles and dissociation duration. Using Redtail Splitfin(Xenotoca Viviparous ff ff Goodeidae eiseni) as a model, the e ects of cryoprotectants (dimethyl sulfoxide, methanol, and glycerol) with di erent Goodeids concentrations (5–15% v/v %), equilibration exposure times (1–60 min), cooling rates (5–40 °C/min), con- 4 6 Endangered species centrations (4 × 10 –4×10 bundles/ml), buffers (HBSS, PBS and NaCl), and buffer osmolalities (200–400 Motility activation mOsmol/kg) were investigated. After cooling and thawing, sperm bundles maintained their packed form. A specific protocol was developed (10% dimethyl sulfoxide, 20-min equilibration, 10 °C/min cooling rate, 4 × 106 bundles/ml, and 300 mOsmol/kg HBSS). This protocol yielded 89 ± 5% of post-thaw dissociable bundles with 209 ± 10 s of dissociation duration for X. eiseni, 96 ± 9% with 814 ± 14 s for Blackfin Goodea (Goodea at- ripinni), and 66 ± 2% with 726 ± 25 s for Striped Goodeid (Ataeniobius toweri). This is the first study of cryopreservation of sperm within bundles for livebearing fishes and provides a basis for establishment of germplasm repositories for goodeids and other livebearers. 1. Introduction and surface waters, basin deforestation, habitat destruction, and in- troduction of exotic species [8]. Additionally, the resulting small po- Fishes of the family Goodeidae are considered to be among the most pulation sizes potentially lead to losses of local populations via demo- at-risk taxa in the world [10]. Goodeidae includes two subfamilies: graphic stochasticity, increasing the risk of extinction due to Empetrichthyinae and Goodeinae. Empetrichthyinae comprises 3 extant inbreeding, decreases in genetic variation, and fixation of deleterious oviparous (egg-laying) species in 2 genera that inhabit small-volume alleles [28]. Therefore, urgent action for conservation of goodeids is springs of the southwestern Great Basin of the United States [33]. The needed. subfamily Goodeinae includes about 45 viviparous (livebearing) species Current efforts toward goodeid conservation include protection and (referred to as ‘goodeids’) in 18 genera inhabiting shallow freshwaters restoration of natural habitats and captive breeding [22]. The goal of within the Central Mexican Plateau [33]. Of these, 12 are critically habitat restoration is to maintain healthy populations and genetic di- endangered, endangered, or vulnerable, and 3 are extinct among 17 versity in historic habitats, however this goal is usually difficult to ac- that have been assessed by the International Union for Conservation of complish and can take decades, with population sizes and genetic di- Nature (IUCN) Red List of Threatened Species [21]. Another assessment versity of concerned species continuing to decline in the wild before full (referred as ‘the 2005 report’) based on 18 years of field research in restoration can be realized [1]. To address the difficulties of reaching combination with a detailed scientific literature survey, suggested that long-term goals, short-term efforts, such as captive breeding, have also about 35 species of goodeids were endangered, threatened, and vul- been initiated to ensure survival and to slow down losses of genetic nerable as of 2005 [6]. The rapid decline of goodeid populations has diversity [25]. However, these approaches are costly, and may cause been attributed to the heavily disturbed aquatic ecosystem in central inbreeding depression, disease outbreaks, and long-term loss of genetic Mexico resulting from water pollution, reductions in levels of ground diversity [29]. Repositories of cryopreserved germplasm can become a ∗ Corresponding author. Aquatic Germplasm and Genetic Resources Center, Louisiana State University Agricultural Center, School of Renewable and Natural Resources, 2288 Gourrier Avenue, Baton Rouge, LA 70820, USA. E-mail address: [email protected] (T.R. Tiersch). https://doi.org/10.1016/j.cryobiol.2018.04.009 Received 9 January 2018; Received in revised form 22 March 2018; Accepted 13 April 2018 Available online 14 April 2018 0011-2240/ © 2018 Elsevier Inc. All rights reserved. Y. Liu et al. Cryobiology 82 (2018) 49–56 viable tool to address these challenges by preserving germplasm for A. toweri. future use at a relatively low cost, ensuring integrity of genetic di- versity, enabling genetic assessment and management, and enhancing 2. Materials and methods captive breeding [26,30]. This tool has been used to improve diversity in recovery of endangered mammals, such as black-footed ferrets 2.1. Fish husbandry (Mustela nigripes)[15], giant panda (Ailuropoda melanoleuca)[20], and Namibian cheetahs (Acinonyx jubatus)[5]. However, it has been ne- Protocols for the use of animals in this study were reviewed and glected in conservation programs of imperiled fishes. For example, in approved by the Louisiana State University Institutional Animal Care our review of about 90 recovery plans for endangered or threatened and Use Committee (Baton Rouge, LA). The X. eiseni, G. atripinnis, and fishes developed by the United States Fish and Wildlife Service since A. toweri used in this study were 2-y old and maintained in the Aquatic 1980s, only 2 mention cryopreservation of germplasm [32]. Germplasm and Genetic Resources Center (AGGRC) at the Louisiana Development of cryopreservation protocols is the basis for the es- State University Agricultural Center (Baton Rouge, Louisiana, USA). tablishment of germplasm repositories [2,3]. Protocols for sperm These fishes were bred from aquarium-trade populations for research cryopreservation of livebearing fishes have been developed for two purposes and were not removed from wild populations. The X. eiseni genera within Poeciliidae. For example, Xiphophorus species have been and G. atripinns were bred by H. Grier [7] and transferred to the AGGRC the most studied due to their importance as cancer research models at < 1-y old. The A. toweri were obtained from the Goodeid Working [35]. Fertilization success was less than 20% when females were in- Group (http://www.goodeidworkinggroup.com). At the AGGRC, fishes seminated with thawed or fresh sperm from X. helleri [41], X. cou- were cultured indoors at 22–26 °C with a 14 h:10 h (light:dark) photo- chianus [38], X. maculatus [39], and X. variatus [40]. Species from the period in 80-l recirculating aquarium tanks (about 30 fish per tank) and genus Poecilia, such as the Guppy (Poecilia reticulata) and the Sailfin fed twice daily with tropical flakes (Pentair Aquatic Eco-systems, FL, Molly (P. latipinna) are popular ornamental fishes and research models. USA) and twice weekly with frozen brine shrimp (Sally's Frozen Brine In these species, fertilization success was ∼50% when females were Shrimp™, San Francisco Bay Brand, CA, USA). Males were mixed at a inseminated with thawed sperm [19]. To date, there are no reports of 2:1 ratio with females in each tank. Additional water quality para- cryopreservation of sperm from goodeids. meters were monitored every 2–4 weeks and held within acceptable Viviparous fishes employ unique reproductive features such as in- ranges including: pH (7–8), ammonia (0–0.1 mg/l), and nitrites ternal fertilization and the bearing of live young [13,34]. Freshwater (0–0.8 mg/l). The X. eiseni were used in Experiments 1–3 as a model for livebearing fishes usually package sperm in bundles (spermato- protocol development, and a generalized protocol was applied to X. zeugmata), which are believed to facilitate the transfer of sperm from eiseni, G. atripinns and A. toweri in Experiment 4. male to female [12]. The viviparity mechanisms of poeciliids and goodeids evolved independently, and thus there are di fferences in sperm bundles between the two groups. For example, bundles from P. 2.2. Collection of sperm bundles reticulata and Xiphophorus species can be dissociated into free sperm by gentle crushing of testes, thus, sperm can be frozen as separate cells Previous studies showed sperm from X. eiseni could not be collected [19,39], and their quality could be evaluated by commonly used by stripping [23]. As such, fish were euthanized by exposure to parameters, such as sperm motility, duration, and velocity. However, 300 mg/l Tricaine methanesulfonate (MS-222, Western Chemical, Inc. bundles from goodeids pose difficulties for sperm cryopreservation. For WA, USA) followed by severing of the spinal column behind the head. example, after testes were crushed, bundle dissociation occurred rarely To eliminate MS-222
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