The endocrine control of embryonic diapause in the Australian sharpnose shark Rhizoprionodon taylori

Waltrick, Daniela de Souza (2013) The endocrine control of embryonic diapause in the Australian sharpnose shark Rhizoprionodon taylori. Masters (Research) thesis, James Cook University.

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Abstract

Embryonic diapause, the temporary suspension of development at any stage of embryogenesis, is a reproductive strategy widespread among all vertebrates, including elasmobranchs. Prolonging the gestation period is believed to be an adaptation to cope with unfavourable environmental conditions and therefore, allowing parturition to occur in conditions that are more suitable for newborns. Although it has only been confirmed in two elasmobranchs (Rhizoprionodon taylori and Dasyatis say), evidence suggests that at least 14 species of rays and two sharks undergo diapause, suggesting this form of reproduction exists within a wide range of reproductive modes, including lecithotrophs and matrotrophs. Where it has been studied, embryogenesis is arrested at the blastodisc stage and preserved in the uterus from four to ten months.

Endocrine systems have remained relatively conserved throughout the vertebrate evolutionary history. Therefore, current models on vertebrates in which diapause have been extensively studied provide the basis to formulate theories for the control mechanisms existent in elasmobranchs. In mammals and reptiles, the ovary represents an important source of steroid hormones for the regulation of reproduction. The corpora lutea is an indispensable gland that mainly produces progesterone (P4), the key hormone associated with gestation in vertebrates. Similar to other taxa, the ovarian follicles of Chondrichthyes may give rise to secondary structures homologous to the corpora lutea by mean of atresia or ovulation. These follicles may be very similar, thus distinguishing these structures may be difficult and problematic, in part because of the confusing literature. Considering the importance of these temporary structures as possible sources of steroid hormones and their control of diapause, ovarian follicles and circulating hormone levels were investigated throughout the reproductive cycle of R. taylori.

Three secondary ovarian follicles occur in the ovary of R. taylori throughout the reproductive cycle. At late diapause, a new ovarian cycle is restarted and atresia may occur at early non-vitellogenic oocytes, giving rise to atretic previtellogenic follicles. During the diapausing period however, a number postovulatory follicles (POF) and usually only one vitellogenic atretic follicle (AF) compose the ovary during the diapausing period. These structures persist in the ovary from 7 to 10 months, however their steroidogenic capacity and possible role in reproduction remain unknown. The macroscopic identification of AF and POF is only possible during part of embryonic diapause due to the relatively different sizes of these structures. However, extrapolation of these characteristics to identify AF and POF i other species is discouraged due to the high morphological variability among species.

This study is the first report of steroid hormones in a diapausing elasmobranch and therefore contributes to a better understanding of the endocrine control of reproductive processes within this group. Levels of 17ß-estradiol (E2), testosterone (T) and P4 are reported in plasma samples of wild female R. taylori captured throughout the reproductive cycle and correlated with internal morphological changes. Levels of P4 and T were elevated through most of the embryonic diapause period, suggesting a role of these hormones in the maintenance of this condition. Increasing T plasma concentrations from late diapause to early active development were associated with a possible role of androgens in the termination of embryonic diapause. As in other elasmobranchs, a concomitant increase of E2 with ovarian follicle size suggested a direct role of this hormone in regulating vitellogenesis. Significant correlations between photoperiod or water temperature and maximum follicular diameter and hepatosomatic index could suggest that these abiotic factors play a role triggering and regulating the synchrony and timing of reproductive events.

Item ID: 29003
Item Type: Thesis (Masters (Research))
Keywords: Rhizoprionodon taylori; elasmobranchs; reproductive strategy; embryonic diapause; suspension of embryo development; embryogenesis; embryogenesis triggers; steroidogenic capacity
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The publication is:

Waltrick, Daniela, Awruch, Cynthia, and Simpfendorfer, Colin (2012) Embryonic diapause in the elasmobranchs. Reviews in Fish Biology and Fisheries, 22 (4). pp. 849-859.

Date Deposited: 29 Aug 2013 05:48
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 100%
SEO Codes: 83 ANIMAL PRODUCTION AND ANIMAL PRIMARY PRODUCTS > 8302 Fisheries - Wild Caught > 830204 Wild Caught Fin Fish (excl. Tuna) @ 100%
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