Elsevier

Theriogenology

Volume 83, Issue 7, 15 April 2015, Pages 1174-1178.e1
Theriogenology

Research article
Timing associated with oviductal sperm storage and release after artificial insemination in domestic hens

https://doi.org/10.1016/j.theriogenology.2014.12.022Get rights and content

Abstract

Female birds store sperm in sperm storage tubules (SSTs) in the uterovaginal junction of their reproductive tract for days or weeks (depending on species) before fertilization. Sperm are transported from the SSTs to the infundibulum where fertilization occurs immediately after ovulation of each ovum. The timing of sperm release from the SSTs relative to ovulation is unknown for any bird. Here, we show that, after artificial insemination of domestic fowl Gallus domesticus, sperm are not accepted into any region of the oviduct before sexual maturity. Once hens reach maturity, there is a temporal shift in the distribution of sperm throughout the oviduct. Sperm are first accepted into and accumulate in the SSTs 6 to 8 days before ovulation but are at this point significantly less numerous in the infundibulum. From 1 to 6 days before ovulation, approximately 10-fold more sperm (235 × 103 sperm) populate the infundibulum than at 6 to 8 days before ovulation (26 × 103 sperm; P < 0.001). Our results suggest that the mechanisms underlying sperm acceptance and release in the oviduct are under fine temporal control, most likely mediated by female hormones.

Introduction

Sperm storage in the oviduct is an essential and probably ubiquitous feature of avian reproduction [1]. Sperm are stored in and released from sperm storage tubules (SSTs) located in the uterovaginal junction, from where they travel to and accumulate in the infundibulum where fertilization occurs. Transport of sperm to the infundibulum is rapid, with some sperm reaching the SSTs within less than one hour of insemination in the domestic fowl Gallus domesticus and turkey Meleagris gallopavo [2], [3]. Because avian ova are ovulated sequentially at intervals of 24 hours (or longer in some species) and can be fertilized only during a short window of approximately 15 minutes after ovulation [4], the release of stored sperm from the SSTs ensures a constant supply in the infundibulum [5], [6].

The duration of sperm storage varies markedly between the bird species, from about 6 days in pigeons to over 2 months in some seabirds [6], [7] and over 3 months in the domestic turkey M gallopavo [8]. Because in some bird species, sperm remain viable from inseminations occurring several months before the onset of laying [9], the oviduct in these species must be sufficiently well developed to contain functional SSTs long before egg laying commences. In the fulmar Fulmarus glacialis, which routinely stores sperm for at least 3 weeks before fertilization, SSTs are present at least 4 weeks before ovulation [7].

In most temperate breeding birds, the reproductive tract of both sexes regresses outside the breeding season and regrows rapidly the next breeding season [10]. The development of the SSTs and the appearance of sperm in the SSTs relative to the onset of laying are known for three passerine birds: the yellow-headed blackbird Xanthocephalus xanthocephalus [11], pied flycatcher Ficedula hypoleuca [12], and zebra finch Taeniopygia guttata [13]. The first two of these are seasonal breeders; the zebra finch (both in the wild and captivity) is an opportunistic breeder and under suitable conditions breeds continuously. When female pied flycatchers and yellow-headed blackbirds first return from migration about 10 days before the onset of egg laying, their oviduct and ovarian follicles are relatively undeveloped but their SSTs are functional [4], [10]. Similarly, in the zebra finch, SSTs are present in the oviduct of unpaired females.

Avian SSTs were first discovered and have been studied in most detail in the domestic fowl [3], [14], [1]. It may therefore seem surprising that the temporal pattern of sperm storage potential relative to the onset of egg laying in the domestic fowl is poorly known. It is known, however, that the domestic fowl, like other birds, can store sperm before the onset of laying and that the uptake of sperm by the SSTs is greater at this time than that when inseminations occur during laying [15], [16], [17]. In this respect, the domestic fowl is similar to other birds that copulate most frequently in the days or, in the case of certain seabirds, weeks, before the onset of egg laying and either cease to copulate or reduce the rate of copulation once egg laying has started [18], [19].

Sperm storage tubule maturation is at least partially regulated by estradiol and progesterone produced in the ovaries, the levels of which vary with female maturity [20], [21], [22], [23]. It therefore follows that female hormones may mediate the uptake and acceptance of sperm into the SSTs.

What remains unknown, for any bird species, is whether sperm accumulate in the SSTs for some time before being released to populate the infundibulum just before ovulation. It seems logical that this is what should occur, especially in seabirds where the interval between the last insemination and fertilization may be several weeks.

The aim of the present study therefore was to establish, using the domestic fowl, (1) the timing of sperm acceptance into the SSTs and (2) the appearance of sperm in the infundibulum relative to the onset of laying.

Section snippets

Materials and methods

Immature female domestic fowl from an egg-type strain (ISA Brown; Institut de Selection Animale, Saint-Brieuc, France) were raised collectively in a floor pen (photoperiod: 8L:16D) at Institut National de la Recherche Agronomique research facilities, Nouzilly (France). At 16 weeks of age, the females were caged individually and subjected to a progressively increasing photoperiod (+2 h/wk from 18 weeks of age, reaching 16L:8D at 22 weeks of age) to stimulate gonad development. Food and water

Results

The number and the distribution of sperm in the different oviduct regions were clearly associated with the degree of sexual maturation. After insemination of 200 × 106 sperm, the oviducts of immature females (8–10 days before laying) were devoid of sperm in all regions, whereas in maturing and mature hens (both pre-lay and laying), large quantities of sperm were recovered from all regions (Fig. 1).

The number of sperm found in each oviduct region was highly dependent on maturity status, as

Discussion

Our results report two key temporal aspects of sperm storage and release in domestic fowl, both of which have important implications for our understanding of these processes in other nondomestic birds. First, sperm acceptance into any region of the oviduct is limited to 8 to 10 days before ovulation. Immature hens, not yet at this stage of sexual development, do not accept or retain any sperm despite the presence of SSTs in the UVJ. Second, there is a 10-fold increase in sperm presence in the

Acknowledgments

The authors thank Frederic Mercerand and his colleagues at Institut National de la Recherche Agronomique (INRA) research facilities, Nouzilly (France) for expert animal care. This work was supported by INRA. Birkhead T.R. and Hemmings N. were funded by a grant from the European Research Council (grant number 268688).

References (33)

  • P.E. Lake

    Gamete production and the fertile period with particular reference to domesticated birds

    Symp Zool Soc Lond

    (1975)
  • Y. Saeki et al.

    Studies on the advance and distribution of cock sperm in the oviduct, with special reference to the tracing method with 32P-labelled sperm

    Bull Nat Inst Anim Ind Chiba

    (1963)
  • M.R. Bakst et al.

    Oviductal sperm selection, transport, and storage in poultry

    Poult Sci Rev

    (1994)
  • T.R. Birkhead et al.

    Sperm competition in birds: evolutionary causes and consequences

    (1992)
  • S. Hatch

    Mechanism and ecological significance of sperm storage in the Northern Fulmar with reference to its occurrence in other birds

    The Auk

    (1983)
  • M.J. Imber

    Breeding biology of the grey-faced petrel Pterodroma macroptera gouldi

    Ibis

    (1976)
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