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The Lamprey Gonad

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Lampreys: Biology, Conservation and Control

Abstract

Understanding gonadal development in lampreys is complicated by their complex life cycle, the long period during which their gonads remain histologically undifferentiated, and their lack of any close living relatives. This chapter synthesizes the available information related to lamprey sex determination, sex differentiation, sexual maturation, and sex steroids, and it identifies key research needs. A detailed review of lamprey sex ratios shows that: (1) adult lampreys (i.e., during the upstream migration or at spawning) exhibit a small but consistent excess of males in virtually all species studied (with significantly female-biased sex ratios noted only in sea lamprey in the three upper Great Lakes following initiation of sea lamprey control); (2) larval sex ratios are generally at parity or with an excess of females; (3) transformers collected above barriers or following lampricide treatment tend to be male biased in the earliest age classes to metamorphose; and (4) there is spatial and temporal variation in sex ratio during the parasitic feeding phase, but overall sex ratio is less male biased than during the adult phase, suggesting that females suffer higher mortality just prior to or during sexual maturation. The shift in sex ratio observed in the upper Great Lakes following initiation of control led to suggestions of environmental sex determination (ESD), specifically density-dependent sex determination, but evidence for ESD in lampreys is equivocal. Sex ratios did not become female biased in the lower Great Lakes, and all five lakes now show a slight excess of males even though abundance has been low and relatively stable for the past several decades. Furthermore, although a significant relationship between larval density and sex ratio has been observed in two non-parasitic species in the southeastern United States, significant relationships between larval density and sex ratio are not evident among contemporaneous sea lamprey populations (i.e., before or after the initiation of control). ESD, usually temperature-dependent sex determination, has been reported in a number of fish species, but no fish species with exclusively ESD have been identified to date. Skewed sex ratios may result from environmental influences on genetic sex determination rather than strict ESD, and the nature of the genotype × environment interactions can differ among populations and over time. However, apart from ruling out “the usual suspects” (i.e., genes implicated in sex determination in other vertebrates), nothing is known regarding the possible genetic basis of sex determination in lampreys. In contrast, many of the genes involved in the sex differentiation process (i.e., development of the undifferentiated gonad into an ovary or testis) tend to be conserved among vertebrates, and initial studies suggest that at least some of the same genes are involved in gonadal development in lampreys. Understanding the factors influencing lamprey sex determination and differentiation has been complicated by lack of knowledge regarding the critical sex differentiation period. Lampreys are sometimes said to pass through an initial female stage or female intersexual stage, because mitosis and meiosis appear to occur in most larvae regardless of future sex. However, meiosis and oocyte growth are more synchronized and extensive in female larvae, and the extent to which oocytes develop and regress in presumptive males either varies among individuals and species or reflects differences in the degree to which these transient processes are detected. Ovarian differentiation is generally thought to be complete at ~1 and 2–3 years of age in non-parasitic and most parasitic lamprey species, respectively, and at 4–5 years in the anadromous sea lamprey. Later and more prolonged mitosis in parasitic species permits elaboration of a larger stock of oocytes, and persistence of a limited number of undifferentiated germ cells in some parasitic species may allow further oocyte recruitment in large larvae. In all species, testicular differentiation occurs at or around the onset of metamorphosis, at which time resumption of mitosis in the remaining undifferentiated germ cells produces spermatogonia. In vivo biopsy studies showed that sea lamprey gonads can remain labile as long as undifferentiated germ cells remain in the gonads (i.e., after the apparent completion of ovarian differentiation, but up until differentiation of the remaining germ cells at the end of the larval stage). The presence of “atypical” gonads (which often developed into typical males in biopsied larvae) in sea lamprey from both the Great Lakes and Atlantic drainages is consistent with delayed gonadal differentiation but requires further study. Despite the apparent lability of the lamprey gonad, hormonal sex control has not been successful. Non-parasitic lampreys begin maturing during the latter stages of metamorphosis; in contrast, parasitic species remain sexually immature until they approach the end of the juvenile feeding phase, and sexual maturation proceeds during the non-trophic spawning migration. Although the rate of maturation varies among species, depending on the duration of migration, all species and life history types appear to converge again during final maturation ~1–2 months before spawning. Oocytes begin to approach their size at maturity (~1 mm in virtually all species), and, at ovulation, the oocytes (now typically called eggs) are synchronously released into the body cavity. The mature ovary constitutes ~25–35% of a female’s total body weight, regardless of species, but the total number of eggs (fecundity) increases approximately with the cubic power of body length so that fecundity in the largest anadromous parasitic species (e.g., mean 172,000 in sea lamprey) is almost two orders of magnitude higher than that of the much smaller non-parasitic species. The mature testis constitutes ~2–10% of a male’s body weight, with gonadosomatic index (GSI) appearing to be higher in males of non-parasitic species compared to parasitic species, although absolute testis size is still much higher in parasitic species. The study of lamprey steroidogenesis and steroid receptors is contributing to our understanding of the evolution of steroid hormones as transcriptions factors in vertebrates, but much still needs to be learned regarding the role of sex steroids in lamprey sex differentiation and sexual maturation.

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Notes

  1. 1.

    Where steroid refers to a molecular structure and hormone refers to a function; not all steroids are hormones (e.g., some are parts of synthetic pathways but do not function as hormones), and not all molecules that function as hormones (e.g., GnRH) are steroids.

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Acknowledgements

We gratefully acknowledge Kristian Sattelberger for helping to prepare the figures and the reference list, Drs. Colin J. Garroway and Alison E. Wright for their input and discussions related to lamprey sex determination, and Drs. John B. Hume and Murray D. Wiegand for providing insightful comments on an earlier draft of this chapter.

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Correspondence to Margaret F. Docker .

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Docker, M.F., Beamish, F.W.H., Yasmin, T., Bryan, M.B., Khan, A. (2019). The Lamprey Gonad. In: Docker, M. (eds) Lampreys: Biology, Conservation and Control. Fish & Fisheries Series, vol 38. Springer, Dordrecht. https://doi.org/10.1007/978-94-024-1684-8_1

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