Biol Reprod Track the topics, authors and articles important to you
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow My Folders
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Shimmin, G.A.
Right arrow Articles by Temple-Smith, P.D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shimmin, G.A.
Right arrow Articles by Temple-Smith, P.D.
Agricola
Right arrow Articles by Shimmin, G.A.
Right arrow Articles by Temple-Smith, P.D.
Biology of Reproduction 60, 1353-1359 (1999)
©Copyright 1999 Society for the Study of Reproduction, Inc.

Articles

Sperm Transport and Storage in the Agile Antechinus (Antechinus agilis)1

G.A. Shimmin2,a, M. Jones3,a, D.A. Taggarta, and P.D. Temple-Smith3,,4,a

a Department of Anatomy, Monash University, Clayton, Victoria 3168, Australia


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
This study was an examination of the timing of ejaculation and the dynamics of sperm transport in the female reproductive tract of the agile Antechinus (Antechinus agilis) and the relationship of these parameters to single and multiple matings. Mating in this species is characteristically long compared with that of other mammals, lasting for up to 8–12 h during which time the pair remain locked together. After the first hour of mating, only ~40% of males had ejaculated, but by the third hour all males had ejaculated. The total number of spermatozoa extracted from the female tract remained at approximately 30 x 103 spermatozoa per side over the next 9 h of copulation. After completion of male/female access (12 h), ~56% of spermatozoa extracted were located in the lower isthmic region of the oviduct where specialized sperm storage crypts are located. The number of spermatozoa extracted from the female reproductive tract did not decline over the next 3 days, but there was a change in the distribution of spermatozoa with an increase in the proportion of extracted spermatozoa stored in the lower isthmus (~76%). However, 7 to 14 days after mating, only ~30% of the stored spermatozoa (~9.4 x 103 spermatozoa per side) were still present in the isthmus. When females were mated with a second male on a consecutive day, the sperm numbers extracted from the tract were about twice that deposited during single mating, with sperm transport to the lower isthmus occurring over a similar time frame. Although the occurrence of extended copulations in the wild has not yet been confirmed, these laboratory results suggest that similar periods of copulation are likely, since completion of the ejaculation process requires at least 3 h. The extended copulation in A. agilis reduces the possibility of an early second mating, which might interfere with the normal transport and crypt colonization of spermatozoa through competition.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Prolonged copulation, in which mating lasts much longer than the time necessary for semen transfer, is recognized as a form of mate guarding (contact guarding) in which the mating male prevents, by behavioral tactics, access by other males to the estrous female [1]. Likewise, extended copulations observed in Antechinus stuartii (= A. agilis) in captivity may act as a form of contact mate guarding, although mating behavior of A. stuartii (= A. agilis) in the wild is poorly understood. The agile Antechinus has been recently recognized as separate species from brown marsupial mouse, Antechinus stuartii, and subsequently reclassified [2]; hereafter in this paper, reference to A. stuartii is intended to refer also to A. agilis. In the agile Antechinus, the average length of copulation in the laboratory is ~6–8 h [3], although 12-h mating periods have been observed [4, 5]. The extended mating times observed in A. stuartii are unusual, even when compared to those of other dasyurid species. The timing of ejaculation during copulation in the agile Antechinus is unknown, although an early deposition would assist transportation of spermatozoa to the oviduct prior to the conclusion of mating.

Successful insemination and transport of spermatozoa to the site of fertilization are important to ensure siring success in all species. Considerable variation exists both within the marsupials and between marsupials and eutherian mammals in this regard [6]. The dynamics of sperm transport in marsupials have been examined in only four species: the tammar wallaby, Macropus eugenii [7]; the fat-tailed dunnart, Sminthopsis crassicaudata [8]; the American opossum, Didelphis virginiana [9, 10]; and the brown marsupial mouse, A. stuartii [5, 11].

After insemination into the urogenital sinus, marsupial spermatozoa are transported through the lateral vaginae and uterus almost immediately as a result of peristaltic contractions of the myometrium [12, 13] and sperm motility [14, 15]. Spermatozoa from A. stuartii were recently shown to have an unusual sinusoidal form of progressive motility [16] that produced a rapid forward progression, resulting in extremely efficient transport of spermatozoa to the oviductal isthmus [5]. Upon reaching the lower isthmic region of the oviduct, sperm from A. stuartii and other dasyurid species are stored in an immotile state, in specialized crypts, for up to 14 days prior to fertilization [4, 5, 8, 17–19].

The promiscuous mating behavior of A. stuartii [20] suggests that sperm competition may occur within the female reproductive tract, especially for access to storage sites in the oviductal crypts and to oocytes at fertilization. No data are available either on the organization of spermatozoa from rival males within the isthmic storage crypts or on the maximum number of sperm that can be stored by the crypts. Selwood and McCallum [19] suggested that second- and third-mating males may be able to contribute sperm for fertilization; this was recently confirmed from observations by Shimmin et al. [21], who showed that multiple paternity occurs within litters of A. stuartii.

The reproductive strategies of agile Antechinus are unusual. Extended periods of sperm storage in the female reproductive tract, coupled with a promiscuous lifestyle, provides an ideal model for the study of mating, sperm transport, and storage. This study was an examination of the timing of ejaculation and the dynamics of sperm transport and storage in A. agilis and the effects of order of mating on these parameters.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Animal Capture and Maintenance

A. agilis were trapped in the Yarra State Forest, approximately 70 km east of Melbourne, Australia (DCNR permit number RP-96-080). After capture, animals were transferred to the Anatomy Department Animal House (Monash University, Clayton; Animal Ethics #95/165). Female A. agilis were housed 3 per cage in standard rat boxes, while males were caged individually in standard mouse boxes. Room temperature was kept at 23°C ± 3°C, and the light cycle was adjusted to mimic natural conditions. All animals were fed a diet of moistened cat chow and newborn rats, with the occasional addition of fruit and mealworms. Water was available ad libitum.

Determination of the Onset of Estrus and Mating Studies

Urine samples were collected from all females three times per week, and the number of cornified epithelial cells was assessed to determine the onset of estrus [17]. Females in estrus were placed into large glass-bottomed tanks in order to monitor intromission. Each female was allowed a 10-min acclimatization/pre-scenting period before a single male was introduced into the tank. Two series of mating experiments were conducted: 1) single mating access and 2) double mating access (Fig. 1). Timing of mating commenced from when intromission was first observed. Females were killed either immediately after separation from the male following the desired duration of mating, or else held for 3–14 days after mating for analysis of long-term sperm storage. Females that were mated twice were mated for up to 12 h on Day 1 of the experiment (completion mating) followed by a 24-h rest period. On Day 2, females were mated to a different male and then either killed immediately after separation (following the appropriate duration of mating) or 5–10 days later.



View larger version (18K):
[in this window]
[in a new window]
  		FIG. 1. The mating access plan indicates time of introduction and separation for each experimental group and any delay before females were killed. All females were in full estrus (high levels of cornified epithelial cells in the urine) at the time of introduction. If mating did not commence almost immediately, animals were separated and any female that had ovulated after the delay was not included in the results. At the conclusion of the designated access period, males were returned to their holding cages. Vertical dotted line, females returned to holding cage; C, animals paired for 12 h (completed mating); open circles, mating commenced; open triangles, mating pair separated, female not mated again; closed circles, female killed and reproductive tract removed; closed triangles, time of separation after first mating access. Exp. 1: Broken line (small), period of mating; broken line (large), female held to assess sperm storage efficiency. Exp. 2: Solid line, first male mating access; broken line (small), period of mating for second male; broken line (large), female held to assess sperm storage efficiency. Data for groups 6 and 9 taken from Taggart [38].

Dissection of the Female Reproductive Tract and Estimation of Sperm Numbers

The reproductive tract was removed carefully and then bisected. One side was prepared for histology (light microscopy), and the contralateral side was divided into five sections: lateral vagina, uterus and uterine neck, lower isthmus, upper isthmus, and ampulla. Each segment was placed in an isolated droplet of MEM (Minimum Essential Medium), and sperm were extracted using the procedure of Taggart and Temple-Smith [5]. The spermatozoa/media mixture from each segment was diluted to a final volume of 0.5 ml with MEM, and the number of spermatozoa was estimated using an improved Neubauer (Weber, London, UK) hemocytometer and a standard counting procedure.

Statistical Analysis

A one-way ANOVA was used to compare sperm numbers within the same segments and total sperm number in the different experimental groups.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Sperm Transport during Single Matings

After 1-h copulation, spermatozoa were present in the reproductive tract of only two of the five females examined. In these two females, a mean of 2 x 103 ± 1 x 103 spermatozoa per side were found (Fig. 2), ~92% of which were located in the lateral vagina (Fig. 3a). Spermatozoa were present in the uterus of one of these females (100 spermatozoa per side) but were absent from the oviduct.



View larger version (31K):
[in this window]
[in a new window]
  		FIG. 2. Stacked graph showing the sperm content of individual reproductive tract segments in the reproductive tract of female A. stuartii at varying time intervals during mating and for specified periods following both single and double matings (mean ± SEM on total sperm number). Group 1: 1-h mating; group 2: 3-h mating; group 3: 6-h mating; group 4: mated to completion (12 h); group 5: mated to completion (12 h, killed after 3 days delay); group 6: mated to completion (12 h, killed after 7–14 days delay); group 7: mated to completion on first day (12 h), mated for 3 h on Day 2; group 8: mated to completion on first day (12 h), mated to completion on second day (12 h) and killed immediately; group 9: mated to completion on first day (12 h), mated to completion on second day (12 h) and killed after 5–10 days delay.



View larger version (31K):
[in this window]
[in a new window]
  		FIG. 3. Number of spermatozoa (mean ± SEM) in individual segments of the female reproductive tract of A. stuartii at varying time intervals after the commencement of a single mating. LV, Lateral vagina; U, uterus; LI, lower isthmus; UI, upper isthmus; A, ampulla. a) Group 1: 1-h mating; b) group 2: 3-h mating; c) group 3: 6-h mating; d) group 4: mated to completion (12 h); e) group 5: mated to completion (12 h, killed after 3 days delay); f) group 6: mated to completion (12 h, killed after 7–14 days delay). * (p < 0.05) Indicates significant change from the sperm number found in the same segment at the previous sample time. Numbers in parentheses indicate the percentage of spermatozoa extracted from each segment.

Ejaculation had occurred for all males 3 h after the commencement of mating. A total of 29 x 103 ± 5 x 103 spermatozoa per side were found in the reproductive tract of females in this group (Fig. 2). The lateral vagina contained ~78% of the extracted spermatozoa (23 x 103 ± 5 x 103 spermatozoa per side), and most of the remaining spermatozoa (~18%, 5 x 103 ± 3 x 103 spermatozoa per side) were located in the uterus (Fig. 3b). Progression of spermatozoa into the lower region of the isthmus had begun in two females only. In these females, only ~4% (1 x 103 spermatozoa per side) of the extracted spermatozoa were found in the isthmus (Fig. 3b).

The total number of extracted spermatozoa within the female reproductive tract after 6-h copulation (29 x 103 ± 2 x 103 spermatozoa per side; Fig. 2) was not significantly different (p > 0.05) from that found in the 3-h group. The number of extracted spermatozoa from the lateral vaginae and uterine segments had not changed significantly (lateral vaginae, ~70%, 20 x 103 ± 15 x 103 spermatozoa per side; uterus, ~14%, 4 x 103 ± 2 x 103 spermatozoa per side). A significant increase (p < 0.05) was observed, however, in the number of spermatozoa extracted from the lower isthmus (5 x 103 ± 2 x 103 spermatozoa per side) (Fig. 3c), which contained approximately ~16% of the spermatozoa extracted from the female reproductive tract at this time.

All matings were completed by 12 h. At this time the total number of spermatozoa extracted from the female reproductive tract was 25 x 103 ± 3 x 103 spermatozoa per side, which was not significantly different (p > 0.05) from the total number of spermatozoa extracted at 3 and 6 h (Fig. 2). However, by this time most extracted spermatozoa (~56%) had advanced to the isthmus (14 x 103 ± 5 x 103 spermatozoa per side; Fig. 3d). The remaining spermatozoa were mostly extracted from the uterus (~33%, 8.4 x 103 ± 3.2 x 103 spermatozoa per side), with a further ~5% of spermatozoa (1.3 x 103 ± 1.0 x 103 spermatozoa per side) extracted from the lateral vagina (Fig. 3d).

The total number of spermatozoa extracted from the female reproductive tract 3 days after the completion of mating was not changed significantly (p > 0.05) in relation to that extracted from the 12-h mating group (35 x 103 ± 13 x 103 spermatozoa per side, Fig. 2). However, significant changes (p < 0.05) in the regional distribution of spermatozoa in the female reproductive tract were observed. The number of spermatozoa extracted from the lateral vaginae and uterine segments had decreased significantly (lateral vaginae: < 1% of spermatozoa in the female reproductive tract or 0.29 x 103 ± 0.13 x 103 spermatozoa per side; uterus: ~20% of spermatozoa in the female reproductive tract or 6.9 x 103 ± 5.6 x 103 spermatozoa per side), and there was a corresponding increase in the sperm content of the lower isthmus (~76% or 27 x 103 ± 8.9 x 103 spermatozoa per side, Fig. 3e).

Seven to fourteen days after the conclusion of mating, the total number of spermatozoa extracted from the female tract had decreased, but not significantly (p > 0.05) (11 x 103 ± 7 x 103 spermatozoa per side, Fig. 2). The proportion of spermatozoa located in the lateral vaginae and uterine segments, however, had decreased significantly in comparison with values in earlier samples (lateral vaginae, 7–14 days, < 1%, 63 ± 63 spermatozoa per side; uterus, 7–14 days, 13.3%, 1.4 x 103 ± 1.4 x 103 spermatozoa per side, Fig. 3f). Although the number of spermatozoa extracted from the lower isthmus (9.4 x 103 ± 5.4 x 103 spermatozoa per side, Fig. 3f) had decreased, this made up a greater proportion of the total number of spermatozoa extracted from the tract (7–14 days, ~87% in the lower isthmus). The numbers of spermatozoa extracted from the upper isthmus never exceeded ~6% of the total number found in the tract of any of the groups, and spermatozoa were found in this region in only 3 of 28 females examined.

Sperm Transport in Double Matings

The values for dynamics of sperm transport following a mating to completion (on Day 1) plus a 3-h second mating (on Day 2) (group 7) (Fig. 4a) were equivalent to the combined data for the 12-h (completion) and 3-h single matings (refer to Fig. 3, b and d). The total number of spermatozoa extracted from females within this group was 39 x 103 ± 7 x 103 spermatozoa per side (Fig. 2). Spermatozoa were relatively evenly distributed between the lateral vagina (~35%, 14 x 103 ± 6 x 103 spermatozoa per side), uterus (~36%, 14 x 103 ± 8 x 103 spermatozoa per side), and the isthmic regions (~29%, 11 x 103 ± 3 x 103 spermatozoa per side, Fig. 4a).



View larger version (17K):
[in this window]
[in a new window]
  		FIG. 4. Number of spermatozoa (mean ± SEM) in individual segments of the female reproductive tract of A. stuartii at varying time intervals after double mating. LV, Lateral vagina; U, uterus; LI, lower isthmus; UI, upper isthmus; A, ampulla. a) Group 7: mated to completion on first day (12 h); mated for 3 h on Day 2; b) group 8: mated to completion on first day (12 h), mated to completion on second day (12 h) and killed immediately; c) group 9: mated to completion on first day (12 h), mated to completion on second day (12 h) and killed after 5–10 days delay. * (p < 0.05) Indicates significant change from the sperm number found in the same segment at the previous sample time. Numbers in parentheses indicate the percentage of spermatozoa extracted from each segment.

In animals that were mated to completion twice on consecutive days (group 8), the total number of spermatozoa extracted from the reproductive tract (65 x 103 ± 14 x 103 spermatozoa per side, Fig. 2) was significantly greater, equivalent to twice the amount of sperm deposited by a single 12-h (completion)-mating male. At the completion of a second mating, most extracted spermatozoa were located in the isthmic regions (35 x 103 ± 16 x 103 spermatozoa per side, ~54%). The uterus contained 19 x 103 ± 11 x 103 spermatozoa per side (~29%), while 10 x 103 ± 9 x 103 spermatozoa per side (~16%) were present in the lateral vagina (Fig. 4b).

The numbers of spermatozoa extracted from the reproductive tract of females killed between 5 and 10 days after the completion of the second mating were not significantly different (p > 0.05) (37 x 103 ± 14 x 103 spermatozoa per side, Fig. 2) from that present at the completion of the second mating. The total number of spermatozoa extracted from the lower isthmus was similar to that found immediately following the second mating (7–14 days, ~88%, 32 x 103 ± 18 x 103 spermatozoa per side), and this represented an increased proportion of the extracted spermatozoa from the female reproductive tract as compared to the proportion in group 8 females (completion + completion) (Fig. 4b).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
This study has shown that the total number of spermatozoa extracted from the female reproductive tract after a single mating increases from 2 x 103 ± 1 x 103 spermatozoa per side 1 h after the commencement of copulation to a maximum of 29 x 103 ± 5 x 103 spermatozoa per side after 3 h of copulation. As the maximum number of spermatozoa found in the female tract is reached 3 h after the commencement of mating, this suggests that ejaculation in A. agilis most likely occurs as a slow release or perhaps a series of bursts between the first and third hour of mating.

A recent study on the mating behavior of male A. stuartii showed that pelvic thrusting, apparent throughout the mating period, became less frequent during the latter stages of copulation [22]. Maximum thrusting activity was observed in the first few hours of mating, which corresponds to the time at which insemination was observed in the current study. Given that semen deposition is complete within the first 3 h of copulation, we suggest that A. agilis have evolved an extended period of mating to contact mate guard the females and that thrusting activity after ejaculation is needed to maintain an erection and perhaps aid sperm transport in the female.

There are currently no field-based studies in A. agilis in which copulation has been examined under natural conditions. However, the high population densities of this species [23], promiscuous lifestyle of both sexes [19], and the long-term storage of spermatozoa in the female reproductive tract suggest that sperm competition is prevalent within natural populations of A. agilis. This hypothesis is supported further by the testis/body weight ratio; that male A. stuartii have a large testis/body weight ratio compared to other marsupials [6]. This reinforces the hypothesis that contact mate guarding is the incentive behind prolonged copulation in agile Antechinus. In addition, by increasing the physical costs associated with mating, males might discourage females from seeking other mates in the days immediately following copulation. This would allow a large proportion of a mating male's sperm to become well established in the oviductal crypts.

The total number of sperm extracted from the female reproductive tract of A. agilis after a single mating remained relatively constant from 3 h of mating to 3 days postcopulation, at approximately 30 x 103 spermatozoa per side. These data support observations by Taggart and Temple-Smith [5], who found a total of 37 x 103 ± 23 x 103 spermatozoa per side in the female reproductive tract 24 h after copulation in A. stuartii. The decline in extracted sperm number observed 7–14 days postmating (60–70% reduction) indicates that sperm are continually lost from the isthmic storage region. The mechanism by which sperm are lost is not clear, but suggestions include a degeneration of crypt-stored spermatozoa, phagocytosis of spermatozoa by crypt cells, and the result of increased numbers of leukocytes [5]. However, fertility studies after extended sperm storage indicate that sufficient spermatozoa remain to ensure that embryo production rate exceeds teat number, as almost all females have all teats occupied by a pouch young following parturition [19].

The large amounts of sperm extracted from the female reproductive tract in the double series of matings (completion + completion, 65 x 103 spermatozoa per side) clearly represent the ejaculate of two males, as twice the amount of sperm was present in the reproductive tract than after a single mating. The high numbers of sperm remaining in the lower isthmus 5–10 days after a second mating indicate the effectiveness of sperm storage in this region.

At the completion of a single mating, ~57% of extracted spermatozoa were from the isthmus, indicating a rapid and efficient transport of spermatozoa through the female tract. The distribution of extracted spermatozoa in the double-mating series shows similar sperm deposition and transportation rates. It is clear from the results for group 7 (comp. + 3 h) that the large number of spermatozoa found in the lower isthmus of double-mated females were derived from the first-mating male on Day 1, whereas those observed in the lateral vagina corresponded to the sperm from the second male. The distribution of spermatozoa after two successive matings to completion can be explained in a similar manner (with twice the number of spermatozoa extracted from the isthmic crypts as compared to the number from a single mating), presumably consisting of spermatozoa from both mating males. These data show that although the number of sperm extracted following insemination is extremely small compared to findings in most other mammals, the transport efficiency is high. This confirms previous observations by Taggart and Temple-Smith [5] that ~60% of extracted spermatozoa were located within the isthmic crypts by 24 h after a single captive mating.

The finding in this study of rapid sperm transport to the oviduct in A. agilis is in contrast to an earlier suggestion by Selwood and McCallum [19] that few spermatozoa reach the oviduct between 1 and 5 days after mating. However, their sperm distribution data 1 day after mating [19] were based on the histological examination, rather than numerical assessment, of the reproductive tract of a single female that was found to have no spermatozoa in the oviduct. Data on sperm distribution in the current study clearly demonstrate ejaculation and an orderly progression of spermatozoa through the reproductive tract toward the isthmus in the initial 3 h of copulation.

The process governing passage of spermatozoa from the site of insemination to the site of fertilization has previously been accepted as relatively ubiquitous among mammals [14, 24, 25]. Transport of spermatozoa through the female reproductive tract of A. stuartii, however, has proven to be an unusual and extremely efficient process that contrasts with the sustained transportation system described in most other mammals [7, 9, 15, 26]. At ejaculation in most mammalian species, large numbers of spermatozoa are deposited in the vagina. These progress through the cervix and uterotubal junction that are thought to act as selective barriers to migrating sperm prior to reaching the isthmus [14, 27]. Although only four studies have examined sperm transport in female marsupials [5, 7–9], most have shown a mode of transportation and colonization similar to that described in eutherian mammals. The cervix and uterotubal junction in most species examined are also thought to serve similar functions [5, 7–9, 28, 29].

Colonization of the oviductal crypts in A. agilis was evident 3 h after the beginning of mating. These data, combined with the high rate of success at which ejaculated spermatozoa reached the isthmus [5], suggest that the cervix and the uterotubule junction provide little if any barrier to sperm transport in A. agilis. The observation by Finemore [30] that the epithelium and lumen of the lateral vaginae in A. stuartii were free of mucus and secretions immediately after copulation is evidence for the absence of a mucus-based sperm reservoir function for the vaginal culs-de-sac and cervix in this species.

The numbers of spermatozoa in the ejaculate of the dasyurids and didelphids that have been examined are significantly lower than for similar-sized marsupials from other families and most eutherian mammals [6]. The ratio of ejaculated spermatozoa to the number present in the oviductal crypts is, however, much higher, indicating that large numbers of ejaculated spermatozoa are not required for successful reproduction in the dasyurid and didelphid marsupials that have been examined [5, 8, 31, 32].

It has been proposed that sperm pairing in the American didelphids aids the efficiency of sperm transport to the isthmus [33, 34]. The unusual sinusoidal motility observed in A. stuartii is also thought to relate to the efficiency of sperm transport through the reproductive tract [16]. The rhythmical movement of the sperm tail produces a rapid forward progression, propelling the spermatozoa through the tract. It has been suggested that sinusoidal motility and the distinctive structural features of the female reproductive tract, in combination, are the main factors that facilitate the highly efficient transportation system observed in A. stuartii.

Promiscuity among female A. stuartii [20] suggests the possibility that spermatozoa from more than one male may colonize the oviductal crypts, creating a competitive situation between the spermatozoa of rival males. It remains unknown, however, how spermatozoa from different males are arranged within the crypts. The order of mating, the time delay between matings, and the mating time in relation to ovulation are all factors that may affect the organization of the sperm in the crypts, and hence the siring success of a particular male [35, 36]. Studies investigating sperm competition in the isthmus of dasyurids are few; however, as shown in a recent study [21] using DNA profiling to determine the siring success of two male A. stuartii given access to one female, males that mated second had a higher siring success. Furthermore, a high rate of mixed-paternity litters was also described in this species by Shimmin et al. [21]. This suggests that the order of copulation is an important factor in determining paternity success for male A. agilis. Efficient transport of spermatozoa to the oviduct and lengthy periods of storage are designed to ensure the success of multiple matings and encourage sperm competition and multiple-paternity litters, which may help to maintain the high levels of heterozygosity observed in wild A. agilis populations [37].


   FOOTNOTES
 
1 This work was supported by an Australian Research Council grant to P.T.-S. (#20-104-013). Back

2 Correspondence. FAX: 61 03 99052766; glenn.shimmin{at}med.monash.edu.au Back

3 Current address: Dept. of Zoology, University of Melbourne, Parkville, Victoria 3052, Australia. Back

4 Current address: Conservation Research Unit, Zoological Board of Victoria, Parkville, Victoria 3052, Australia. Back

Accepted: January 19, 1999.

Received: August 3, 1998.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Sherman PW. Mate guarding as paternity insurance in Idaho ground squirrels. Nature 1989; 338:418–420.[CrossRef][Medline]
  2. Dickman CR, Parnaby HE, Crowther MS, King DH. Antechinus agilis (Marsupialia:Dasyuridae), a new species from the A. stuartii complex in south-eastern Australia. Aust J Zool 1998; 46:1–26.
  3. Marlow BJ. Reproductive behavior of the marsupial mouse Antechinus flavipies (Waterhouse) (Marsupalia) and the development of pouch young. Aust J Zool 1961; 9:203–218.
  4. Woolley PA. Reproduction in Antechinus spp and other dasyurid marsupials. Symp Zool Soc Lond 1966; 15:281–294.
  5. Taggart DA, Temple-Smith PD. Transport and storage of spermatozoa in the female reproductive tract of the brown marsupial mouse, Antechinus stuartii (Dasyuridae). J Reprod Fertil 1991; 93:97–110.[Abstract/Free Full Text]
  6. Taggart DA, Breed WG, Temple-Smith PD, Purvis A, Shimmin GA. Reproductive mating strategies and sperm competition in marsupials and monotremes. In: Birkhead T, Moller A (eds.), Sperm Competition and Sexual Selection. London: Academic Press; 1997: 623–665.
  7. Tyndale-Biscoe CH, Rodger JC. Differential transport of spermatozoa into the two sides of the genital tract of a monovular marsupial, the tammar wallaby (Macropus eugenii). J Reprod Fertil 1978; 52:37–43.[Abstract/Free Full Text]
  8. Breed WG, Leigh CM, Bennett JH. Sperm morphology and storage in the female reproductive tract of the fat-tailed dunnart, Sminthopsis crassicaudata (Marsupialia:Dasyuridae). Gamete Res 1989; 23:61–75.[Medline]
  9. Rodger JC, Bedford JM. Induction of oestrus, recovery of gametes and the timing of fertilization events in the opossum, Didelphis virginiana. J Reprod Fertil 1982; 64:159–169.[Abstract/Free Full Text]
  10. Rodger JC, Bedford JM. Separation of sperm pairs and sperm-egg interaction in the opossum, Didelphis virginiana. J Reprod Fertil 1982; 64:171–179.[Abstract/Free Full Text]
  11. Selwood L. A review of the maturation and fertilization in marsupials with special reference to the dasyurid: Antechinus stuartii. In: Archer M (ed.), Carnivorous Marsupials. Australia: Roy Zool Soc NSW; 1982: 65–76.
  12. Hartman CG. Observations on the motility of the opossum genital tract and the vaginal plug. Anat Rec 1924; 27:293–303.
  13. Hughes RL, Rodger JC. Studies on the vaginal mucus of the marsupial Trichosurus. Aust J Zool 1971; 19:19–33.
  14. Drobnis EZ, Overstreet JW. Natural history of mammalian spermatozoa in the female reproductive tract. Oxf Rev Reprod Biol 1992; 14:1–45.[Medline]
  15. Taggart DA. A comparison of sperm and embryo transport in the female reproductive tract of marsupial and eutherian mammals. Reprod Fertil Dev 1994; 6:451–472.[CrossRef][Medline]
  16. Taggart DA, Temple-Smith PD. An unusual mode of progressive motility in spermatozoa from the dasyurid marsupial, Antechinus stuartii. Reprod Fertil Dev 1990; 2:107–114.[Medline]
  17. Selwood L. A timetable of embryonic development of the dasyurid marsupial Antechinus stuartii (Macleay). Aust J Zool 1980; 28:649–668.
  18. Bedford JM, Breed WG. Regulated storage and subsequent transformation of spermatozoa in the fallopian tubes of an Australian marsupial, Smithopsis crassicaudata. Biol Reprod 1994; 50:845–854.[Abstract]
  19. Selwood L, McCallum F. Relationship between longevity of spermatozoa after insemination and the percentage of normal embryos in the brown marsupial mouse (Antechinus stuartii). J Reprod Fertil 1987; 79:495–503.[Abstract/Free Full Text]
  20. Scott MP, Tan TN. A radiotracer technique for the determination of male mating success in natural populations. Behav Ecol Sociobiol 1985; 17:29–33.
  21. Shimmin GA, Taggart DA, Temple-Smith PD. Sperm competition increases reproductive fitness in brown marsupial mice (Antechinus stuartii, Southern Form). In: 4th International DNA Fingerprinting Conference; 1996; Melbourne, Australia. p. 117.
  22. Shimmin GA, Taggart DA, Temple-Smith PD. Mating behavior in brown marsupial mice. In: 42nd Scientific Meeting of the Australian Mammal Society; 1996; Melbourne, Australia. p. 39.
  23. Lee AK, Cockburn A. The Evolutionary Ecology of Marsupials. Cambridge: Cambridge University Press; 1985.
  24. Overstreet JW. Transport of gametes in the reproductive tract of the female mammal. In: Hartmann JF (ed.), Mechanism Control of Fertilization. New York: Academic Press; 1983: 499–543.
  25. Overstreet JW, VandeVoort CA. Sperm transport in the female genital tract. In: Asch RH (ed.), Gamete Physiology. Norwell, MA: Serono Symposia USA; 1990: 43–52.
  26. Hunter RHF, Nichol R, Crabtree SM. Transport of spermatozoa in the ewe: timing of the establishment of a functional population in the oviduct. Reprod Nutr Dev 1980; 20:1869–1875.
  27. Harper MJK. Gamete and zygote transport. In: Knobil E, Neill J (eds.), The Physiology of Reproduction. New York: Raven Press; 1988: 103–134.
  28. Morgan CF. Sexual rhythms in the reproductive tract of the adult female opossum and the effect of hormonal treatments. Am J Anat 1946; 78:411–463.
  29. Risman GC. The effects of estradiol and progesterone on the reproductive tract of the opossum and their possible relation to the parturition. J Morphol 1947; 81:343–397.
  30. Finemore J. Antechinus as a model species for the development of artificial insemination techniques in marsupials. Melbourne, Australia: Dept. of Zoology, University of Melbourne, in conjunction with the Department of Anatomy, Monash University; 1995. Honours Thesis.
  31. Bedford JM, Rodger JC, Breed WG. Why so many mammalian spermatozoa? A clue from marsupials. Proc Roy Soc Lond B Biol Sci 1984; 221:221–233.[Medline]
  32. Taggart DA, Temple-Smith PD. Comparative epididymal morphology and sperm distribution studies in dasyurid marsupials. J Zool (Lond) 1994; 232:365–381.
  33. Biggers JD, Creed RFS. Conjugate spermatozoa of the North American opossum. Nature 1962; 196:1112–1113.
  34. Moore HD, Taggart DA. Sperm pairing in the opossum increases the efficiency of sperm movement in a viscous environment. Biol Reprod 1995; 52:947–953.[Abstract]
  35. Ginsberg JR, Huck UW. Sperm competition in mammals. TREE 1989; 4:74–79.
  36. Roldan ER, Gomendio M, Vitullo AO. The evolution of eutherian spermatozoa and underlying selective forces: female selection and sperm competition. Biol Rev 1992; 67:551–593.[Medline]
  37. Lambert K, Jones M, Shimmin G, Sofronidis G, Bowden D, Taggart D, Temple-Smith P. Informative enzyme/probe combinations for DNA fingerprinting marsupials. Electrophoresis 1997; 18:1688–1692.[Medline]
  38. Taggart DA. Aspects of the reproductive biology and life history of the Dasyuridae (Marsupialia). Melbourne, Australia: Department of Anatomy, Monash University; 1990. Ph.D Thesis.




This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow My Folders
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Shimmin, G.A.
Right arrow Articles by Temple-Smith, P.D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shimmin, G.A.
Right arrow Articles by Temple-Smith, P.D.
Agricola
Right arrow Articles by Shimmin, G.A.
Right arrow Articles by Temple-Smith, P.D.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS