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Canid Reproductive Biology: Norm and Unique Aspects in Strategies and Mechanisms

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Canid Reproductive Biology: Norm and Unique Aspects in Strategies and Mechanisms animals Review Canid Reproductive Biology: Norm and Unique Aspects in Strategies and Mechanisms Jennifer B. Nagashima * and Nucharin Songsasen Center for Species Survival, Smithsonian Conservation Biology Institute, 1500 Remount Rd., Front Royal, VA 22630, USA; [email protected] * Correspondence: [email protected] Simple Summary: The family Canidae, composed of dog-like species such as wolves, foxes, and jackals, demonstrates a significant variety in reproductive biology. In general, female canids expe- rience very long periods of ovarian inactivity during the year; however, there are diverse patterns with regard to seasonality between species, as well as within an individual species depending on geographic region or housing status. Understanding of these differences is critical to the development of assisted reproductive technologies for canid conservation efforts. This review summarizes the current knowledge of canid reproduction, including reproductive cyclicity, seasonal breeding, male sperm traits, and recent developments in assisted reproductive technologies for canids. Abstract: The reproductive physiology of canids is unique compared to other mammalian species. Specifically, the reproductive cycle of female canids is characterized by extended periods of proestrus and estrus followed by obligatory diestrus and protracted ovarian inactivity (anestrus). Although canid reproduction follows this general pattern, studies have shown variations in reproductive biology among species and geographic regions. Understanding of these differences is critical to Citation: Nagashima, J.B.; the development of assisted reproductive technologies including estrus induction, gamete rescue, Songsasen, N. Canid Reproductive and embryo production techniques for canid conservation efforts. This review summarizes current Biology: Norm and Unique Aspects knowledge of canid reproduction, including estrus cyclicity, seasonality, and seminal traits, with in Strategies and Mechanisms. the emphasis on species diversity. The application of reproductive technologies in wild canid Animals 2021, 11, 653. https:// conservation will also be discussed. doi.org/10.3390/ani11030653 Academic Editor: Alberto Keywords: Canidae; seasonality; estrus; assisted reproductive technologies Maria Luciano Received: 18 January 2021 Accepted: 20 February 2021 1. Introduction Published: 1 March 2021 Including the domestic dog, the canid family consists of 37 extant species, five of which are listed as “endangered” or “critically endangered” by the International Union Publisher’s Note: MDPI stays neutral of Conservation of Nature (IUCN) (Figure1a). Furthermore, 1/3 of wild canid species with regard to jurisdictional claims in are in decline due to increased anthropogenic activities, such as agricultural development, published maps and institutional affil- whereas two species, including the coyote (Canis latrans) and golden jackal (Canis aureus) iations. are abundant with increasing population trends (Figure1b). Reproductive sciences play critical roles in species conservation and management [1,2]. Specifically, advances in the understanding about species’ reproductive biology may permit the development of reproductive technologies that are useful for ensuring genetic and Copyright: © 2021 by the authors. demographic viability of ex situ wildlife populations [1]. Such knowledge can also assist in Licensee MDPI, Basel, Switzerland. the development of strategies to control overpopulated wildlife species [1]. Yet, reproduc- This article is an open access article tive biology has not been studied in more than 90% of mammals on the planet, and the distributed under the terms and knowledge gained from “well-studied” species have highlighted remarkable diversity in conditions of the Creative Commons reproductive mechanisms, even among related species [3]. For example, within the Genus Attribution (CC BY) license (https:// Canis, the domestic dog (Canis familiaris) displays non-seasonal reproduction, whereas creativecommons.org/licenses/by/ their wild cousins, including grey wolf (Canis lupus), red wolf (Canis rufus), and coyote are 4.0/). Animals 2021, 11, 653. https://doi.org/10.3390/ani11030653 https://www.mdpi.com/journal/animals Animals 2021, 11, x FOR PEER REVIEW 2 of 23 Animals 2021, 11, 653 2 of 23 whereas their wild cousins, including grey wolf (Canis lupus), red wolf (Canis rufus), and coyote are seasonal breeders, and dingo [4] (Canis lupus dingo) exhibits variable reproduc- seasonaltive seasonality. breeders, Though and dingo the domestic [4](Canis dog lupus serves dingo) asexhibits a critical variable baseline reproductive for the reproductive seasonal- ity.physiology Though of the the domestic taxon as dog a whole, serves investigatio as a criticalns baseline on species-specific for the reproductive differences physiology are crit- ofical the for taxon the development as a whole, investigations of reproductive on technologies species-specific for differencesmanaging endangered are critical for canid the developmentpopulations. Comparison of reproductive of reproductive technologies forseasonality, managing puberty, endangered and parental canid populations. behaviors Comparisonacross Canidae of have reproductive previously seasonality, been reviewed puberty, [5]. andHowever, parental there behaviors are also acrossseveral Canidae aspects haveof domestic previously dog reproduction been reviewed that [5 ].as-yet However, elude thereunderstanding, are also several including aspects the mechanisms of domestic dogof estrus reproduction resumption that and as-yet egg maturation elude understanding, prior to fertilization. including In the this mechanisms review, we of summa- estrus resumptionrize current andknowledge egg maturation of canid prior reproductive to fertilization. biology, In thiswith review, the emphasis we summarize on species current di- knowledgeversity, and of the canid application reproductive of reproductive biology, with technologies the emphasis in wild on species canid conservation. diversity, and the application of reproductive technologies in wild canid conservation. a 1 b 4 5 11 3 6 25 17 CR En NT LC Decreasing Stable Increasing Unknown Figure 1. (a) Numbers of wild canid species listed as critically endangered (CR), endangered (En), near threatened (NT) or least concern (LC) status according to the IUCN red list of endangered species; (Figureb) Numbers 1. (a) Numbers of canid species of wild with canid decreasing, species listed stable, as cr increasingitically endangered or unknown (CR), population endangered trends. (En), near threatened (NT) or least concern (LC) status according to the IUCN red list of endangered 2.species; Canid (b Reproductive) Numbers of canid Biology species with decreasing, stable, increasing or unknown population trends.The current knowledge about reproductive biology of the canid family is mostly gleaned from the studies in the domestic dog [6–8]. Generally, female canids are monestrus with2. Canid the reproductiveReproductive cycle Biology characterized by an extended period of proestrus and then estrusThe (~1 current week each).knowledge The estrousabout reproductive period is characterized biology of the by canid an estrogen family peakis mostly that coincidesgleaned from with the rising studies circulating in the domestic progesterone dog concentration,[6–8]. Generally, prior female to ovulation canids are [6, 8mon-–13]. Estrusestrus with is followed the reproductive by diestrus, cycle a luteal characteri phasezed averaging by an extended 2 months pe inriod duration of proestrus irrespective and ofthen pregnancy estrus (~1 [6 ,week14]. Diestrus each). The is succeeded estrous period by anestrus, is characterized an extended by (2–10an estrogen months) peak interval that ofcoincides ovarian with quiescence rising circulating [6]. The reproductive progesterone cycle concentration, of most wild prior canids to isovulation consistent [6,8–13]. to that ofEstrus the domestic is followed dog by where diestrus, diestrus a luteal is followed phase averaging by an extended 2 months period in duration of ovarian irrespective inactivity. However,of pregnancy peripubertal [6,14]. Diestrus bush dogsis succeeded (Speothos by venaticus anestrus,) housed an extended in zoological (2–10 months) institutions interval can undergoof ovarian multiple quiescence estrous [6]. The cycles reproductive without the cycle anestrous of most period wild [canids15]. Seasonal is consistent polyestrous to that cyclesof the domestic have also dog been where shown diestrus in captive is followed dholes (Cuon by an alpinus extended) and period New Guinea of ovarian singing inactiv- dog (ity.Canis However, dingo hallstromi peripubertal) where bush females dogs ( enterSpeothos estrus venaticus when) thehoused prior in breeding zoological attempt institutions does notcan resultundergo in pregnancy multiple estrous [16–18]. cycles While femalewithout domestic the anestrous dogs and period most [15]. wild Seasonal canids ovulate poly- spontaneouslyestrous cycles have in the also absence been shown of a male, in captive there is dholes evidence (Cuon that alpinus the Island) and foxNew (Urocyon Guinea littoralissinging )[dog19 ](Canis and maned dingo hallstromi wolf (Chrysocyon) where brachyurusfemales enter)[20 estrus,21] are when induced the prior ovulators breeding and requireattempt the does presence not result of a in male pregnancy for estrus [16–18]. and/or While ovulation female to occur. domestic To date, dogs the and mechanisms most wild ofcanids
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