Sex differentiation and gonadogenesis in lampreys (Parts I and II)

Abstract

The development of the gonads has been studied in ammocoetes of the landlocked sea lamprey, Petromyzon marinus. Up to lengths of about 70 mm, the gonads remain undifferentiated: the germ cells proliferating to form first small groups and finally large cysts of germ cells. At lengths of 70 to 80 mm, over 70% of all gonads examined were of the cystic type. Measurements made on large numbers of animals at this stage indicate the presence of two distinct groups with smaller and larger gonads. These represent the future male and female gonads respectively. These size differences are thought to correspond to differences in germ cell numbers in the two sexes. In a few cases the sex of the gonads can be distinguished at lengths of 71 to 80 mm, but differentiation is not generally complete below lengths of 100 mm. Differentiation is preceded or accompanied in both sexes by the appearance of growing oocytes. The frequency distribution for oocyte counts in bimodal, the lower numbers representing the future male gonads. During auxocytosis and differentiation large numbers of germ cells undergo degeneration; the majority at the zygotene or pachytene stage. In definitive females, the surviving oocytes represent only 20 to 30% of the total number of germ cells in the cystic gonad. Oogenesis begins within the cysts which are broken up by the invasion of somatic elements. The presence of large cysts is therefore without relevance to the future sex of the gonad.The extensive regression of germ cells in the future male gonads results in an actual decrease in size during differentiation. The somatic characters that distinguish the earlier male gonads of Lampetra planeri are less developed in marinus. In size and histological structure these often resemble the undifferentiated gonads of earlier larval stages. The male germ cells are derived from residual undifferentiated elements which survive the extensive regression at the cystic stage. At first the male gonads contain only a few isolated germ cells which proliferate slowly throughout larval life. At metamorphosis there is a very marked acceleration in the division of the male germ cells. Male germ cells retain their undifferentiated character throughout the larval period. In regard to the mode,of sex differentiation marinus is more differentiated than planeri. This is supported by the existence of a sex dimorphism in gonad size (and probably germ cell numbers) preceding morphological and histological differentiation, and by the evidence of bimodality in oocyte numbers. The vastly reduced fecundity of the brook lamprey compared with that of the sea lamprey is associated with significant differences in the pattern and phasing of gonad development in the two species. In planeri, germ cell proliferation begins earlier than in marinus, but is shorter in duration, terminating in auxocytosis and differentiation. This results in an enormous reduction in the total numbers of germ cells. Expressed as a percentage of the total numbers, the proportion undergoing regression during sex differentiation is thought to be similar in both species. The difference in the number of germ cells which survive as oocytes in the female gonads of the two species is thus a direct consequence of precocious oocyte development and the earlier curtailment of the gonial divisions in the brook lamprey ammocoete.