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BOR - Papers in Press, published online ahead of print May 19, 2004.
Biol Reprod 2004, 10.1095/biolreprod.103.019919
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BIOLOGY OF REPRODUCTION 71, 1036–1042 (2004)
DOI: 10.1095/biolreprod.103.019919
© 2004 by the Society for the Study of Reproduction, Inc.

Ovary

Ovarian Aging in Two Species of Long-Lived Rockfish, Sebastes aleutianus and S. alutus1

Jan-Peter de Bruin4, Roger G. Gosden5, Caleb E. Finch2,3, and Bruce M. Leaman6

Andrus Gerontology Center and Department of Biological Sciences,3 University of Southern California, Los Angeles, California 90089 Department of Endocrinology and Fertility,4 University Medical Centre Utrecht, 3584 CX Utrecht, The Netherlands The Jones Institute for Reproductive Medicine,5 Eastern Virginia Medical School, Norfolk, Virginia 23507 International Pacific Halibut Commission,6 Seattle, Washington 98145


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Little is known about the ovary during aging in long-lived fish with respect to follicular stages and de novo oogenesis. We examined two species of rockfish, Sebastes aleutianus (rougheye rockfish) and Sebastes alutus (Pacific ocean perch). Fish were sampled offshore of British Columbia, age was estimated by otolith annuli, and the ovaries were examined histologically. In S. aleutianus, age up to 80 yr did not markedly alter the frequency distribution of oocytes, follicles, or their total numbers. Similarly, in a larger sample of S. alutus, the abundance of oocytes and follicles showed little age trend up through 77 yr. However, fish older than 50 yr lacked the largest and smallest oocyte size classes (40–60, >80 µm) and the smallest follicle size class (200– 350 µm), which results from the later seasonal developmental state of these older fish. These data provide evidence that oogenesis continues at advanced ages in these two species, in contrast with long-held assumptions about mammals. These species represent an iteroparous extreme in the spectrum of life history strategies and merit investigation to determine the mechanisms for such an extended reproductive life span.

aging, oocyte development, ovary, ovulatory cycle, seasonal reproduction


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Aging is widely associated with decreases in reproduction, although the extent of change and the causes vary by gender and species [1–3]. Declining fertility in males is seldom a limiting factor in population fertility because male fertility generally continues at ages beyond which female fertility declines or ceases [2]. As a rule in mammals, the ovary acquires its full store of primordial follicles by birth and, as a consequence of atresia, fewer than 50% of the original stock of primary follicles and oocytes remain at puberty. In humans, rhesus monkeys, and certain strains of laboratory rodents, detailed studies show the complete loss of follicles, oocytes, and fertility during mid- or late life [1–4]. So far, few exceptions to this strong trend have been found; for example, in certain prosimians, thymidine-labeling studies indicate some persistence of de novo oogenesis into adult ages [5], although late-formed oocytes may not contribute to fertility. In contrast to the mid-life loss of fertility in some mammals, the grey mouse lemur, chimpanzee, and domestic dog retain fertility until shortly before natural death at advanced ages [2–4], but there is no evidence of de novo oogenesis in adults of any of these species. To the contrary, a recent paper [6] claims to provide evidence that germline stem cells exist in the postnatal mouse ovary and, even more surprisingly, that they are continuously active in replenishing gametes, by analogy with the testis and the ovary in many lower vertebrates and invertebrates.

Much less is known about de novo oogenesis in adults of nonmammalian vertebrates. Histological studies of two relatively short-lived birds, the domestic quail and chicken, do not indicate de novo oogenesis in young adults, and there is evidence of declining ovulatory function with age [7, 8]. In contrast, oocytes in germinal beds showed extensive thymidine incorporation in sexually mature turtles aged 1 yr, which is a strong indicator of de novo oogenesis [7]. The oldest frogs examined (13 yr, which is near the recorded maximum life span of 15 yr) still produced full-size clutches of ova in response to gonadotropin treatment [9]. These examples suggest that reproductive aging and de novo oogenesis in adults may vary widely by species. Evidence of longer reproductive life span (in both absolute years and relative to total life span) in the more primitive vertebrate groups therefore presents an evolutionary sequence of interest. Fish are particularly interesting for comparative studies of reproductive aging because of their huge range of life spans and reproductive schedules, ranging from the semelparous Pacific salmon, with life spans in the upper range of laboratory rodents [2], to many deep-living Pacific Ocean fish, which can live up to or beyond the upper limit of human life span [2, 10–21]. Individual ages in feral fish populations can be assessed accurately by the annual otolith rings, as calibrated by natural radioisotopic decay, e.g., in various rockfish species of the genus Sebastes [10, 11, 14, 15, 18], from the northeast Pacific, and in the orange roughy [19, 20], and warty oreo [21] from the southwest Pacific. The genus Sebastes includes, where the populations have not been exploited, many species in which individual life spans far exceed those of most mammals. For example, specimens of S. aleutianus have lived up to at least 205 yr [12, 13, 18], which greatly exceeds the human 122-yr record life span of Jeanne Calment, who lived 70 yr after menopause [22].

The Sebastes we examine in this paper are very long-lived teleosts, and their reproduction in relation to age has not been detailed previously. In many teleosts, the ovary is considered to generate a new crop of oocytes each year though continuing de novo oogenesis in adults [21–28]. Seasonally recurrent oogenesis is well studied in trout (Salmo), which mature much earlier and have a shorter average life span than Sebastes [26, 27]. In contrast, lampreys (Agnatha) are thought to complete oogenesis before their only season of spawning [2, 24]. Other iteroparous fish may also lack de novo oogenesis as adults, according to limited histological data [24, 25].

For further insights into the diversity of reproductive aging manifested in mammals, it is essential to evaluate ovaries of Sebastes at advanced ages. As a first approach, we examined oocyte and follicle size classes in samples of S. aleutianus and S. alutus of determined ages. We describe the size distribution of oocytes and follicles present in the ovaries of mature fish of different ages sampled simultaneously. The specimens were divided into three age groups in which the oldest (>50 yr) represent advanced ages, as expected from previous studies [12].

These deep-caught specimens died during removal to the surface because, like most other physoclistous fish, Sebastes cannot equilibrate its swim bladder under decompression from depths. Thus, it is impossible to trace the sizes of a developmental series from primary oocyte to mature follicle or to describe the ontogenetic progression of oocyte or follicle sizes for individual fish of these species as they age. Whereas the available fish differed according to the season of sampling for our study (see Methods), both species have the same seasonal cycles of ovarian oocyte maturation and follicle growth, with the maximum follicular development in October–November, followed by spawning in February–March [28]. Spawning is followed by a brief period of ovarian recovery (April–May) during which any unspawned larvae or atretic follicles are resorbed, and which precedes the development of a new crop of oocytes beginning in June. Seasonal timing is important with regard to the interpretation of the characteristics of oocytes and follicles examined in this first report of age-specific reproductive development in long-lived fish species.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Collection and Characterization of Specimens

Sebastes aleutianus (rougheye rockfish) and S. alutus (Pacific ocean perch) were collected by bottom trawls offshore of British Columbia, Canada, from a Canadian Department of Fisheries and Oceans research vessel. All fish were treated in accordance with approved departmental policies on the care and treatment of animals during scientific research. These policies conform to both Canadian National Research Council and U.S. National Academy of Sciences policies on animal care. Animals were killed as rapidly as possible to minimize suffering.

Both Sebastes species have the same annual reproductive cycle, with spring spawning. However, it was not feasible to collect both species in the same season. Sebastes aleutianus was collected off the west coast of the Queen Charlotte Islands from a single trawl haul at depths of 341– 360 m in June 1995. Sebastes alutus was collected from single hauls off the west coast of the Queen Charlotte Islands, Vancouver Island, and southern Hecate Strait at 260–357 m in November 1985. Note that these different seasons of collection represent different stages of the annual cycle of oocyte and follicle development (dates are given because of possible historical trends). S. aleutianus was sampled several months after spawning, whereas S. alutus was sampled before spawning, when preovulatory follicles are at maximum development.

The age of each specimen was estimated by counting the annular growth zones on cross sections of the sagittal otoliths, a method that has been validated by tetracycline marking and by natural radioisotopic ratios [10, 11]. Otoliths were sectioned transversely through the center, the transverse face burned over an alcohol flame, and swabbed with vegetable oil to enhance the contrast between the seasonal growth zones (summer is translucent; winter, opaque) [11, 12].

Specimens were classified into three age groups: young (0–30 yr), middle (31–49 yr), and old (≥ 50 yr) (Table 1). The youngest age group represented the age of sexual maturity to 30 yr. For S. alutus, this grouping included ages from 9–30 yr; for S. aleutianus, ages from 19–30 yr. The youngest age range represented for S. alutus is lower than for S. aleutianus because the latter matures at a later age and we include only mature fish in the analysis [28]. The maximum ages in these samples were 77 yr for S. alutus and 80 yr for S. aleutianus.


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  		TABLE 1. Sample numbers for S. aleutianus and S. alutus collections

Histology

Histological preparations differed as appropriate for the different oocyte/follicle maturational stages at the time each species was sampled. Ovaries of S. alutus were fixed first in Smith formal dichromate and then transferred to buffered formalin for storage. The initial fixation method was chosen to achieve optimal fixation on the larger follicles in these samples and not distort measurements for comparison with the S. aleutianus samples. Sebastes aleutianus ovaries, at an earlier stage, were fixed in buffered formalin. Samples from each species were embedded in paraffin wax and sectioned at 6 µm. Samples were taken from 6–10 locations across each ovary to obtain representative data of follicle profiles. For both species, sections were stained with Harris hematoxylin, counterstained with alcoholic eosin, and mounted on slides for examination. Ovaries of S. alutus were analyzed by B.M.L.; S. aleutianus specimens were analyzed using an image analyzer by J.-P. de B. and R.G.G.

For examination of S. alutus ovaries, we used the primary rectilinear axes of the slides as a common standard, and all mature follicles and immature oocytes were counted along the axes. The diameters of 20 each mature follicles and immature oocytes along the axes, which were sectioned through the nucleus, were measured using a calibrated ocular micrometer on a Leitz compound microscope (Leica Microsystems, Wetzlar, Germany). The seasonal cycle of oocyte and follicular development has been described previously in detail for this genus [16, 29, 30]. and we follow the characterizations and classification scheme of these earlier studies.

For S. aleutianus, 10 random microscopic fields were chosen for image analysis using the IBAS system (Kontron Elektronik, Dusseldorf, Germany). This method was chosen over standard ocular micrometer measurements to obtain sufficient precision with the generally smaller size of follicles in the S. aleutianus samples. The slides were coded to avoid observer bias. The images obtained by a Zeiss photomicroscope (Carl Zeiss, Oberkochen, Germany) at 50x magnification were captured on a 512 x 512 frame. All identifiable follicles and oocytes were selected on the basis of their contrast and morphology. The numbers and diameters deduced from area measurements were estimated for both follicles and oocytes and assigned to a database.

Statistics

Descriptive statistics and analysis of oocyte and follicle distributions were conducted with standard analytical software (SYSTAT v10.0.; SPSS Inc., Chicago, IL). Differences in follicle and oocyte frequency among ages and age groups were examined with one-way ANOVA. The same software was used for linear and nonlinear regressions, fitted to data sets using distance-weighted least squares algorithms, to examine follicle and oocyte relationships with age.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Seventeen samples of mature S. aleutianus, ranging in age from 19 to 80 yr, and 248 samples of mature S. alutus, ranging in age from 9 to 77 yr, were obtained for analysis. For comparison between the species, fish were assigned to categories of young (0–30 yr), middle (31–49 yr), and old (≥50 yr).

S. aleutianus (Rougheye Rockfish)

Most follicles and oocytes were in smaller size classes (≤75 µm) (Figs. 1 and 2), consistent with the time of year and prior spawning (see Methods). Age up to 80 yr did not significantly alter the percentage distribution of either oocytes or follicles (Fig. 2, A and B). There was no significant correlation between the density of oocytes or follicles (number per 2-mm optical field) and age (R2 = 0.08 for oocytes and 0.13 for follicles) (Tables 1 and 2). Nor was there any histological indication of follicular atresia or ovarian pathology. Atresia would be evidenced by hypertrophy of the follicular granulosa as well as dissolution and resorption of the follicle lipids.



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  		FIG. 1. A) Histological section of S. aleutianus ovary, illustrating developing follicles. B) Histological section of mature S. alutus ovary with primary oocytes and developed follicles



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  		FIG. 2. S. aleutianus: Ovarian characteristics in three age groups. Error bars are standard errors. A) Oocyte size class (diameter, µm) frequency distributions. B) Follicle size class (diameter, µm) frequency distributions


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  		TABLE 2. S. aleutianus: Density (number per 2-mm diameter optical field) of ovarian oocytes and follicles in three age groups

S. alutus (Pacific Ocean Perch)

The larger sample size for S. alutus (248 fish) permitted more detailed analysis of potential age effects on ovarian characteristics (Table 3 and Figure 3). Regression of mean follicle abundance and diameter with age indicated significant relationships (P < 0.0005 for both). Similarly, mean oocyte frequency was significantly related to age (P < 0.0005). However, the mean diameter of oocytes was not significantly dependent on age (P = 0.1308). We examined age effects further by looking at the relationship of oocyte and follicle size classes with grouped ages. The oldest age group (≥50 yr) lacked the largest and smallest size classes of oocytes (40–60 µm, >80 µm), as well as the smallest size class of follicles (<350 µm) (Figs. 1 and 4, A and B). For the two younger age groups, the mean frequency of these largest oocytes was greatest in the group aged 31–50 yr, while the youngest group had the highest frequency of the smaller two oocyte size classes. Analysis of variance of the relationship of size classes of oocytes and follicles using age groups as the independent variable also revealed significant positive relationships for frequencies but not mean sizes (Table 3). Follicular atresia was detected in about 0.1% of all follicles examined (53/51 000) [16].


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  		TABLE 3. Analysis of variance results for examination of mean oocyte and follicle frequency and diameter (µm) by age group for S. alutus.*



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  		FIG. 3. Relationship of mean oocyte (upper panels) and follicle (lower panels) numbers and diameters with age in S. alutus. All regressions are significant except that of oocyte diameter and age



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  		FIG. 4. S. alutus: Ovarian characteristics in three age groups. Error bars are standard errors. A) Oocyte size class (diameter, µm) frequency distributions. B) Follicle size class (diameter, µm) frequency distributions

The relationship between both round weight (body weight with viscera included) and ovary weight with age in S. alutus is nonlinear (Fig. 5). Ovarian weight showed an inverted-U distribution with age, such that younger and older fish had smaller ovarian weight than middle-aged fish (Fig. 5A). This relationship resembles, but is slightly more accentuated, than the relationship of age and body length (Fig. 5C) and round weight (body weight including the viscera) (Fig. 5B). Thus, the older fish were slightly smaller, consistent with smaller ovarian mass. Fecundity (number of ova) showed an inverted-U distribution with age (Fig. 5D), similar to that for length and age. Whereas fecundity as a function of weight was essentially linear, it showed marginally greater R2 values when described by a power function (0.431 vs. 0.462, respectively).



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  		FIG. 5. S. alutus. Gross morphological data by age. A) Ovary weight (g). B) Round weight (total wet body weight including viscera, g). C) Body length (cm). D) Fecundity (numbers of eggs per individual)


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Two species of Sebastes were compared at similar ages, from young adults to advanced ages through 80 yr. Very old fish were a minority in these samples from both species, as expected from previous samples [14–16]. In unexploited populations of these species, with natural mortality rates in the 2–5%/yr range for the two species, between 8–30% of a year class survives to age 50 yr and only 1–14% to age 100 yr. The record maximum age estimated for S. aleutianus is 205 yr [11, 13, 15], which is over twofold greater than our oldest fish at 80 yr; for S. alutus, the record of 98 yr [11, 13, 15] is much closer to the 77 yr age of our oldest specimen.

The most striking finding in this study was that the oldest fish in both species had active ovaries with follicular and oocyte enlargement. No female mammal is known to retain fecundity beyond 70 yr because the fixed store of ovarian follicles becomes depleted [1–4]. In S. aleutianus, the normal range of oocyte and follicle size classes was found in all adult ages. All ages had small-sized follicles and oocytes ≤75 µm (Fig. 1), as expected from the summer time of collection when the next crop of eggs is still growing. However, in the larger sample of S. alutus, the older fish conspicuously lacked the largest and smallest oocyte size class and also the smallest follicle size class. It is believed that this apparent deficit is due to the schedule of sampling relative to seasonal ovarian development, as discussed below.

Follicular atresia was uncommon in S. alutus (about 0.1% of follicles). Although no atresia was found in S. aleutianus, the smaller sample size does not allow firm conclusions to be drawn. Because follicular atresia is observed in other fish, e.g., rainbow trout [31] and electric ray [32], S. aleutianus might also show atresia with larger samples but the relatively low level of atresia in S. alutus, with adequate sampling, suggests atresia may be uncommon in these species. In mammals, the incidence of atresia in antral follicles can be reduced experimentally by unilateral ovariectomy or by administration of FSH, which increase the numbers of mature oocytes produced by the remaining ovary [33, 34]. In rainbow trout, unilateral ovariectomy also increased the crop of mature oocytes [27], but it is unclear whether this was due to decreased atresia or increased de novo oogenesis.

The present data cannot resolve whether the apparent ovarian deficit in the largest size group of oocytes in S. alutus is due to senescence. An alternate and more logical explanation than senescence is that the effect can be accounted for simply by the stage of ovarian development of the fish during November, when the specimens were collected. This period is late in the development cycle, immediately prior to ovulation. Because only a single batch of follicles is ripened per year and older/larger fish in this genus and others mature earlier in a given year [35–37], it is probable that all follicles had passed beyond this smallest follicle size class at the time of sampling for these older fish. Because older fish begin to mature oocytes and follicles earlier than young ones, the absence of both the largest oocytes and smallest follicles in the oldest fish is consistent with a relatively later stage of development. We note that the frequency of the middle size class of oocytes in the oldest age group is not significantly different from that in the middle age group. Because only a single follicle crop is produced each year, it is not possible for the later stages of follicle development to be present had the requisite larger oocyte size class not been present at an earlier seasonal period. Resolution of this question could be achieved with serial sampling during the annual reproductive cycle in fish of different ages; however, this process is not possible for the species reported here because of the barotrauma associated with capture from great depths, which causes death from swim bladder rupture.

Rainbow trout also show substantial individual variations in oocyte diameters when sampled 3–4 mo before spawning [26]. Further sampling of different individuals of S. alutus during spring spawning may resolve whether the absence of the largest oocytes observed here is merely due to a seasonal effect or to ovarian senescence.

Other reports indicate that at least some species of poikilothermic vertebrates retain a capacity for oogenesis at advanced ages, in contrast with virtually all mammals (see Introduction). Feral turtles provide further examples. In longitudinal studies of Blanding turtle [38, 39], the fecundity at 60 yr is at least as high as at 20–30 yr; remarkably, the oldest turtles continued to produce viable eggs, as judged by the number hatched and the body size at hatching [38]. Two other turtle species also retain full egg production capacity at advanced ages [40, 41]. Measurement of hormones during the reproductive season can be informative about fertility potential [42].

For those vertebrates with reproduction extending into advanced decades, demographic data are insufficient to evaluate whether mortality rates accelerate at later ages, which is a criterion for senescence at the population level [2, 43–46]. Assessment of senescent mortality is also complicated by the large differences in abundance of individual cohorts in these species, where 20-fold differences in cohort strengths are common. The presence or absence of older individuals of specific ages is therefore dependent on the relative strength of the cohorts present at the time of sampling. The oldest S. alutus tend to be smaller (round and ovarian weights, and length) in association with an inverse relation of survival and growth rates [15]. We do not know if genetic diversity within the populations contributes to these different growth schedules. In the guppy, a freshwater fish, genetic influences on the age and size at maturation and fecundity in natural populations arise from size-class predation [47]. Many species of Sebastes share similar mean follicle sizes across a wide range of ages, which suggests strong selection for optimum packaging of oocytes/ follicles in this genus. However, it is also significant that older S. alutus, despite being shorter and lighter than their middle-aged counterparts, have higher proportions of larger follicles. Previous studies of this species have shown that these older but smaller individuals also have slightly higher egg dry weight than their larger, middle-aged counterparts [16]. This relationship implies an increased probability of reproductive success at advanced ages (assuming gamete quality is equivalent), which is contrary to the trends for reproductive senescence in mammals [2–4].

These data should encourage further study of how some species achieve great longevity with minimal, or even negligible, reproductive senescence. Direct experimental observations on de novo oogenesis in Sebastes may be feasible through thymidine labeling of adult ovaries in short-term organ culture; however, it will be more difficult to evaluate the viability of eggs at advanced ages.

Investigations of the cytogenetics and molecular development of follicles in Sebastes species could give insights on the causes of aneuploidy and follicular atresia in mammalian ovaries. It has long been suspected that cumulative damage in long-lived oocytes is responsible for the age-related loss of oocyte quality, for the decline of fertility, and for increased Down syndrome with maternal age in our species. In contrast to Sebastes, formation of new oocytes in mammals has been thought to be confined to prenatal ages, although this doctrine has recently been challenged by new data [6], and a lively debate is ensuing [48–50]. In consequence, ovarian biology of lower vertebrates may take on new significance if germline stem cells are present and active in postnatal mammalian ovaries. Whereas laboratory study of Sebastes spp. is impractical due to death from swim bladder rupture, nonetheless, the gonadal tissue from these species should be viable for study of oogenesis and meiosis in vitro [48, 49]. Comparative biology will then have to address the question of why human ovaries are peculiarly vulnerable to age changes, both in respect of the depletion of oocytes by midlife and the early deterioration of oocyte quality and rising incidence of aneuploidy [51].


   FOOTNOTES
 
1 Portions of this work supported by the Canadian Department of Fisheries and Oceans and by NIH grants AG-00729 and AG-14571 to C.E.F. Back

2 Correspondence: Caleb E. Finch, Andrus Gerontology Center, 3715 McClintock Ave., University of Southern California, Los Angeles, CA 90089. FAX: 213 740 0853; cefinch{at}usc.edu Back

Received: 5 August 2003.

First decision: 21 August 2003.

Accepted: 28 April 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Gosden RG. The Biology of Menopause. New York: Academic Press; 1985
  2. Finch CE. Longevity, Senescence, and the Genome. University of Chicago Press; 1990
  3. Vom Saal FS, Finch CE, Nelson JF. The natural history of reproductive aging in humans, laboratory rodents, and selected other vertebrates. In: Knobil E (ed.), Physiology of Reproduction, vol. 2, 2nd ed. New York: Raven Press; 1994;61:1213–1314
  4. Finch CE, Sapolsky RM. The evolution of Alzheimer disease, the reproductive schedule, and apoE isoforms. Neurobiol Aging 1999 20:407-428[CrossRef][Medline]
  5. Kumar TC. Oogenesis in adult prosimian primates. Contrib Primatol 1974 3:82-96[Medline]
  6. Johnson J, Canning J, Kaneko T, Pru JK, Tilly J. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 2004 428:145-149[CrossRef][Medline]
  7. Callebaut M, Van Nassauw L, Harrisson F. Comparison between oogenesis and related ovarian structures in a reptile, Pseudemys scripta elegans (turtle) and in a bird Coturnix coturnix japonica (quail). Reprod Nutr Dev 1997 37:233-352
  8. Zuckerman S. The Ovary. New York: Academic Press; 1962
  9. Brocas J, Verzar F. The aging of Xenopus laevis, a South African frog. Gerontologia (Basel) 1961 5:228-240
  10. Bennett JT, Boehlert GW, Turekian KK. Confirmation of longevity in Sebastes diploproa (Pisces: Scorpaenidae) from 210Pb/226Ra measurements in otoliths. Mar Biol 1982 71:209-215[CrossRef]
  11. Chilton DE, Beamish RJ. Age determination methods for fishes studied by the Groundfish Program at the Pacific Biological Station. Can Spec Publ Fish Aquat Sci 1982 60:102
  12. Leaman BM, Beamish RJ. Ecological and management implications of longevity in some northeast Pacific groundfishes. Bull Int North Pacific Commn 1984 42:85-97
  13. Munk KM. Maximum ages of groundfishes in waters off Alaska and British Columbia and considerations of age determination. Alaska Fish Res Bull 2001 8:12-21
  14. Leaman BM, Nagtegaal DA. Age validation and revised natural mortality rate for yellowtail rockfish. Trans Am Fish Soc 1987 116:171-175[CrossRef]
  15. Mulligan TJ, Leaman BM. Length-at-age analysis: can you get what you see?. Can J Fish Aquat Sci 1992 49:632-643
  16. Leaman BM. Reproductive and population biology of Pacific Ocean perch (Sebastes alutus (Gilbert)). University of British Columbia; 1998. Dissertation
  17. Cailliet GM, Ferry L, Love MS, Leaman BM. Report on Aging and Senescence in Fishes. Report for Grant WASC-3-1744. Tiburon, CA: U.S. National Marine Fisheries Service; 1994
  18. Cailliet GM, Andrews AH, Burton EJ, Watters DL, Kline DE, Ferry-Graham LA. Age determination and validation studies of marine fishes: do deep-dwellers live longer?. Exp Gerontol 2001 36:739-764[CrossRef][Medline]
  19. Fenton GE, Short SA, Ritz DA. Age determination of orange roughy Hoplostethus atlanticus using 210Pb:226Ra disequilibria. Marine Biol 1991 109:197-202[CrossRef]
  20. Smith DC, Fenton GE, Robertson SG, Short SA. Age determination and growth of orange roughy (Hoplostethus atlanticus): a comparison of annulus counts with radiometric aging. Can J Fish Aquat Sci 1995 52:391-401
  21. Stewart BD, Fenton GE, Smith DC, Short SA. Validation of otolith-increment age estimates for a deepwater fish species, the warty oreo Allocyttus verrucosus, by radiometric analysis. Marine Biol 1992 123:29-38[CrossRef]
  22. Allard M, Lèbre V, Robine J-M. Jeanne Calment: From Van Gogh's Time to Ours, 122 Extraordinary Years. New York: Freeman Press; 1998
  23. Franchi LL, Mandl AM, Zuckerman S. The development of the ovary and the process of oogenesis. In: Zuckerman S (ed.), The Ovary, vol. 1. New York: Academic Press; 1962:1–88
  24. Tokarz RR. Oogonial proliferation, oogenesis, and folliculogenesis in nonmammalian vertebrates. In: Jones RE (ed.), The Vertebrate Ovary: Comparative Biology and Evolution. New York: Plenum Press; 1971: 145–179
  25. Prisco M, Ricchiari L, Andreuccetti P. An ultrastructural study of germ cells during ovarian differentiation in Torpedo marmorata. Anat Rec 2001 263:239-247[CrossRef][Medline]
  26. Tyler CR, Sumpter JP, Witthames PR. The dynamics of oocyte growth during vitellogenesis in the rainbow trout (Oncorhynchus mykiss). Biol Reprod 1990 43:202-209[Abstract]
  27. Tyler CR, Pottinger TG, Santos E, Sumpter JP, Price SA, Brooks S, Nagler JJ. Mechanisms controlling egg size and number in the rainbow trout, Oncorhynchus mykiss. Biol Reprod 1996 54:8-15[Abstract]
  28. Westrheim SJ. Reproduction, maturation and identification of larvae of some Sebastes (Scorpaenidae) species in the northeast Pacific Ocean. J Fish Res Board Can 1975 32:2399-2411
  29. Moser HG. Reproduction and development of Sebastodes paucispinis and comparison with other rockfishes off southern California. Copeia 1967; 4:773–797
  30. Moser HG. Seasonal histological changes in the gonads of Sebastodes paucispinis Ayres, an ovoviviparous teleost (Family Scorpaenidae). J Morphol 1967 123:329-353[CrossRef][Medline]
  31. Billard R. The reproductive cycle of male and female brown trout (Salmo trutta fario): a quantitative study. Reprod Nutr Dev 1987 27:29-44
  32. Chieffi Baccari G, Minucci S, Di Matteo L, Chieffi G. Ultrastructural investigation of the corpora atretica of the electric ray, Torpedo marmorata. Gen Comp Endocrinol 1992 86:72-80[CrossRef][Medline]
  33. Bast JD, Greenwald GS. Acute and chronic elevations in serum levels of FSH after unilateral ovariectomy in the cyclic hamster. Endocrinology 1977 100:955-966[Abstract/Free Full Text]
  34. Gosden RG, Telfer E, Faddy MJ, Brook DJ. Ovarian cyclicity and follicular recruitment in unilaterally ovariectomized mice. J Reprod Fertil 1989 87:257-264
  35. Eltink ATGW. Changes in age-size distribution and sex ratio during spawning and migration of western mackerel (Scomber scombrus L). J Cons CIEM 1987 44:10-22
  36. Dawson WA. Changes in western mackerel (Scomber scombrus) spawning stock composition during the spawning season. J Mar Biol Assoc U K 1986 66:367-383
  37. Love MS, Morris P, McRae M, Collins R. Life history aspects of 19 rockfish species (Scorpaenidae: Sebastes) from the Southern California Bight. NOAA Technical Report NMFS 87; 1990
  38. Congdon JD, Gibbons JW. Structure and dynamics of a turtle community over two decades. In: Cody MC, Smallwood J (eds.), Long-Term Studies of Vertebrate Communities. New York: Academic Press; 1996:137–159
  39. Congdon JD, Nagle RD, Kinney OM, van Loben Sels RC. Hypotheses of aging in a long-lived vertebrate, Blanding's turtle Emydoidea blandingi. Exp Gerontol 2001 36:813-828[CrossRef][Medline]
  40. Tucker JK, Moll D. Growth, reproduction, and survivorship in the red-eared turtle, Trachemys scripta elegans, in Illinois with conservation implications. Chelonian Conserv Biol 1997 2:352-357
  41. Miller JK. Escaping senescence: demographic data from the three-toed box turtle, Emydoidea blandingii. Exp Gerontol 2001 36:829-832[CrossRef][Medline]
  42. Nisbet IC, Finch CE, Thompson N, Russek-Cohen E, Proudman JA, Ottinger MA. Endocrine patterns during aging in the common tern (Sterna hirundo). Gen Comp Endocrinol 1999 114:279-286[CrossRef][Medline]
  43. Nisbet IC, Apanius V, Friar MS. Breeding performance of very old common terns. J Field Ornithol 73: 117–124; 2002
  44. Rose MR. The Evolutionary Biology of Aging. New York: Oxford University Press; 1991
  45. Charlesworth B. Evolution in Age-Structured Populations, 2nd ed. Cambridge UK: Cambridge University Press; 1994
  46. Vaupel JW, Carey JR, Christensen K, Johnson TE, Yashin Al, Holm NV, Iachine IA, Kannisto V, Khazaeli AA, Liedo P, Longo VD, Zeng Y, Manton KG, Curtsinger JW. Biodemographic trajectories of longevity. Science 1998 280:855-880[Abstract/Free Full Text]
  47. Reznick DN, Shaw FH, Rodd FH, Shaw RG. Evaluation of the rate of evolution in natural populations of guppies. Science 1997 275:1934-1937[Abstract/Free Full Text]
  48. Gosden RG, Mullan J, Picton HM, Yin H, Tan SL. Current perspective on primordial follicle cryopreservation and culture for reproductive medicine. Hum Reprod Update 2002 8:105-110[Abstract/Free Full Text]
  49. Picton HM. Oocyte maturation in vitro. Curr Opin Obstet Gynecol 2002 14:295-302[CrossRef][Medline]
  50. Gosden RG. Germline stem cells in the postnatal ovary—is the ovary like a testis?. Hum Reprod Update 2004 10:1-3[Free Full Text]
  51. Pellestor F, Andreo B, Anral F, Humeau C, Demaille J. Maternal aging and chromosomal abnormalities: new data drawn from in vitro unfertilized human oocytes. Hum Genet 2003: 112:195–203



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