Fish Physiology and Biochemistry vol. 11 no. 1-6 pp 147-154 (1993) Kugler Publications, Amsterdam/New York
Adaptations versus accommodations: some neuroendocrine aspects in teleost fish Y.-A. Fontaine Laboratoirede Physiologie ginirale et compare du Museum national d'Histoire naturelle; Unite' d'Endocrinologie compare associee au C.N.R.S. Paris,France
I. Ambiguities of adaptation Broadly speaking an adaptation is a favourable adjustment to the environment. It represents both a process and a result, which give rise to a first ambiguity. In biology, adaptation occurs in two very different situations. On the one hand, individuals adjust to changing environments using morphofunctional modifications which are often called "physiological adaptations". On the other hand, in the course of evolution, organisms acquire hereditary characters (adaptations) which are favourable - given the environment - for their survival and reproduction. These hereditary characters include physiological elements. This ambiguity reflects the independent developments of evolutionary biology and of physiology since Darwin (1859) and Cl. Bernard (1879). It raises - or should raise - a problem to comparative physiologists, i.e., those who take into account species diversity (Prosser 1973) and who take an interest in specific diversity of functions and their regulations. One may feel that to complain about the use of the same word - adaptation - in two different contexts is simply a semantic argument. But I would argue that this confusion hinders any attempt to compare the physiological adjustments involved in the two situations and, hence, to analyze their relationship. Here, I will reserve the use of the word adaptation to its evolutionary meaning, i.e., to the hereditary characters which favour the adjustment of one
species to its environment. As to the adjustments which occur throughout the life span of an organism in response to environmental changes, several items have been proposed, such as "acclimation", "acclimatization" (Prosser 1973). Here I will use "accommodation" (Cuenot 1925). Clearly, accommodations depend on adaptations; the ability to accommodate is itself an adaptation. In order to analyze more precisely the articulation between adaptations and accommodations (see Fig. 1) as well as the diversity of adaptations, we shall consider a few examples of physiological adjustments involving the neuroendocrine system in teleost fish.
II. Responses to environmental changes A. Stress syndrome Any environmental change is likely to evoke stress syndrome. This is an excellent example of the semantic problem and will be briefly considered here for this reason. Indeed, since Selye (1950), stress syndrome is known as the "general adaptation syndrome" (GAS) whereas, in the terminology used in this paper, the various reactions to aggressions are typical accommodations. In fish as in other vertebrates, stress syndrome includes several steps (Pickering 1981; Colombo et al. 1990). Catecholaminergic systems and the hypothalamus-pituitary-interrenal axis are the main agents of the primary alarm reaction, which may in-
148
Result
ADAPTATION (1) (hereditary character involved in adjustement to the environment)
Process
ADAPTATION (2)
ACCOMMODATION (not
hereditary)
ACCOMMODATION (occuring in response to environmental change)
(Time scale)
(Evolution)
(1) An adaptation includes both genomic characters from them. It conditions (-->) the accomodation.
(Life span)
and the phenotypic characters which directly derive
(2) The adaptation process raises a number of questions which will not be discussed here (see GOULD and LEWONTIN, 1979; LEVIN, 1982). Fig. 1. Diversity of the biological adjustments to the environment.
clude the participation of other hormones such as prolactin (Avella et al. 1991). Catecholamines and cortisol may elicit a great diversity of responses (Mazeaud and Mazeaud 1981). The favourable character of certain responses is questionable, as, for instance, osmoregulation is disturbed by stress. However most of them, concerned with metabolism as well as with respiratory and cardiovascular systems, are accommodations which can favour "fight or flight" and then help the fish to cope with environmental challenges. Miinck et al. (1984) have suggested that, in mammals, one function of the pituitary-adrenal activation may be to prevent an overshoot of the various defence mechanisms (Miinck et al. 1984). The existence of GAS in most vertebrates suggests that the adaptations which underly it were acquired early in vertebrate evolution. A first set could be concerned with the neuronal systems controlling adrenocorticotropin cells, catecholaminergic neurons and chromaffin cells. It is worth noting that in rainbow trout groups of cortisol "high responders" and "low responders" could be selected for breeding purposes (Pickering and Pottinger, in Colombo et al. 1990). Another set of adaptations is certainly concerned with the nature of catechola-
mine and cortisol targets. The expression, or a nonexpression, of receptor in a given tissue will qualify it, or not, as a hormonal target. This is a powerful potential process of adaptation as it may lead to important changes in the overall stress response. It is possible that specific differences in hormonal receptors present in adipose tissue could explain the old conflictory data on the lipase response to stress and hormones (Mazeaud and Mazeaud 1981). The identification of actual adaptations underlying GAS would need more comparative data on species differing in their stress response and their ecoethological habits.
B. Adjustment to salt water (1) Accommodations All events induced by salinity changes are accommodations. Let us consider, for instance, the transfer of a teleost fish from fresh water to salt water. Osmosis leads to water loss and ion invasion that the fish will oppose by increasing drinking and ion secretion through epithelia, mainly gills. The ion secretion is carried out in a special cell type, the chloride cells, where it is driven by NaK ATPase
149 (Foskett 1987). In fresh water two types of chloride cells ( and ) are present; upon transfer to salt water, a cells degenerate whereas the a cells undergo hypertrophy and a new type, the accessory cells, appear (see Pisam and Rambourg 1991). Many endocrine systems participate in the accommodation process as shown by various experimental approaches (measurement of plasma hormone level or secretion rate, study of hormone effects). Short and long term regulations have been described. Several hormones (angiotensin, catecholamines, somatostatin, urotensins, glucagon, vasoactive intestinal peptide) are involved in rapid regulation (see Foskett 1987). Only slow acting hormones (mainly cortisol, prolactin - PRL - growth hormone - GH - and triiodothyronine - T 3) will be considered here. Changes in the metabolism of these hormones occur after salt water transfer: increased cortisol production and plasma GH, decreased plasma PRL (see Hirano 1991), increased T3 utilisation and thyroxine (T4 ) deiodination into T3 (Lebel 1991). Accommodating effects of GH and cortisol have been demonstrated on survival, on ion exchanges or on Na+K + ATPase (e.g., Bolton et al. 1987; McCormick and Bern 1989; Boeuf et al. 1990; Madsen 1990). The effect of GH is at least partly mediated by T 3, probably due to stimulation of T4 deiodination (Lebel and Leloup 1992). The hormonal control of chloride cell changes is still to be defined even though effects of cortisol (e.g., Laurent and Perry 1990), GH (e.g., Madsen 1990) and PRL (e.g., Herndon et al. 1991) on morphology and number of chloride cells have been demonstrated. Foskett (1987) suggested that cortisol and GH stimulate the differentiation and the division of chloride cells, respectively, while PRL exerts a dedifferentiating effect. (2) Adaptations The salinity range in which a fish is able to accommodate depends on the species, from stenohaline to euryhaline ones. Even within euryhaline fish which can live in fresh or in sea water (SW) - the efficiency of euryhalinity is variable: some fish can only perform a progressive accommodation whereas others can survive direct transfer.
The different abilities to accommodate are due to different underlying adaptations which can occur at different sites (e.g., control of hormone secretion and properties of chloride cells). GH and PRL cells may be controlled not only by hypothalamic factors but also by other pituitary cells and directly by plasma osmolality (Nishioka et al. 1988). The sensitivity of these cells to plasma osmolality may be an adaptive character. In vitro, rainbow trout PRL cells appear less sensitive to medium osmolality than PRL cells from other, non-salmonids, euryhaline fish (Gonnet et al. 1988). The capacity to differentiate several types of chloride cells (see above) is certainly a major adaptation to euryhalinity. It would be interesting to know if this capacity involves endocrine components such as the presence of certain hormonal receptors in various types of chloride cells. A diversity of adaptations is probably involved in euryhalinity. The identification and understanding of these adaptations require more comparative data on species with different degrees of euryhalinity and different life strategies. This diversity of adaptations is likely to reflect the diversity of the evolutionary processes which gave rise to the present euryhaline species. It is interesting to examine the distribution of euryhaline species within teleost phylogeny (Lauder and Liem 1983). The great majority of euryhaline species are distributed in two rather distantly related groups. The first includes two closely related orders: Elopomorpha and Clupeomorpha in which are found the great migrators, such as Salmo salar, Anguilla sp., Alosa sp.. The second group includes two very closely related orders: Atherinomorpha and Percomorphawhich include a number of well known euryhaline species (Gillichthys, Gobius, Mugil, Platichthys, Tilapia). It can be postulated that euryhalinity was first acquired in populations which happened to live in estuarine zones, this adaptation being obviously favourable for their survival. Then a second step would have been to take advantage of it to use fresh and sea water to a much larger extent as it is the case in the present great amphihaline migrators. In salmonids and clupeids (to which belong Alosa sp.) this organization of the life cycle is somewhat flexible and wholly freshwater species also exist (Thorpe 1987; Hoar 1988).
150 III. Complex life strategies The species which will be considered here have acquired complex life strategies in the course of evolution. Their environmental requirements became different for different stages of the life span such as larval and adult forms or growth and reproduction. Before discussing the examples of salmonids and eels, I will briefly mention the obvious case of classical metamorphosis. Metamorphosis of flatfish (Paralichthys)for instance corresponds to a complete ecological change from a pelagic to a benthic life. Metamorphosis represents, at least partly, expression of adaptations to the new environment. As for amphibians, thyroid and interrenal hormones appear to be involved in flatfish metamorphosis (Miwa et al. 1988; de Jesus et al. 1990). A. Salmonids Salmonids, all of which spawn in fresh water, show a great diversity in their life strategies (Thorpe 1987) and in the efficiency of their euryhalinity (Hoar 1988). Typical migratory species, such as the Salmo salar,grow in fresh water, as parrs, for a few years and then migrate to the sea in defined areas where a second phase of growth occurs. After some years, fish accomplish a second migration back to the area where they were born; the sexual maturation occurs during the freshwater anadromous migration. When young salmons enter in sea water, they accommodate according to the general pattern which was previously described. However the process occurs more readily than in certain other euryhaline fish and even certain other salmonids because they have undergone a kind of metamorphosis called smoltification. Although external factors may modulate or synchronize the time of smoltification, this is clearly a programmed developmental event (M. Fontaine 1975; Hoar 1988; Boeuf 1992). This metamorphosis involves a diversity of changes, especially of adaptations (i.e., of changes concerned with the ability to adjust to the environment). Important osmoregulatory changes occur so that, contrarily to parrs, smolts may be transferred to sea water without problems. This is certainly related to the spectacular changes occurring at the level of
chloride cells where accessory cells appear (Pisam et al. 1988). As mentioned before, in most euryhaline fish this differentiation occurs as accommodation upon transfer to sea water and depends on hormones, mainly GH and cortisol. The differentiation of accessory cells during smoltification may also be secondary to increases in GH and cortisol (which have indeed been observed, see Dickhoff et al. 1990). In any case one can see here an interesting example where similar events have completely different triggers, either a developmental clock (adaptation) or an environmental change (accommodation). Smolts in fresh water acquire characters of sea water fish. For this reason smoltification has often been called a preadaptation (an ambiguous term because it is used in another meaning in evolutionary biology (Lewin 1982)); it is indeed an anticipatory adaptation (see M. Fontaine 1983, 1991). On another hand, osmoregulatory changes lead to a maladaptation to fresh water which together with other changes (e.g., behavioural) trigger the catadromous migration (see M. Fontaine 1975, 1983, 1991; Thorpe 1987; Hoar 1988; Boeuf 1992). One should not forget that smoltification includes a number of changes related to still other functions (e.g., diverse metabolisms, see M. Fontaine 1975; Hoar 1988; Specker 1988; Boeuf 1992). They prepare the fish to the migration. They can be considered as secondary adaptations to the optimal environmental conditions of growth such as they have been retained in the course of the evolution. Smoltification, like more classical metamorphosis, probably depends on thyroid and steroid hormones, the plasma levels of which increase during the parr to smolt transformation (see Specker 1988; Dickhoff et al. 1990; Boeuf 1992). In an interesting generalization, Specker (1988) suggested that a fundamental role of thyroid hormones would be to "preadapt" animals to exploit new food sources. Finally smoltification is a reversible adaptation. If smolts are kept in fresh water they lose their high capacity to accommodate to sea water (Hoar 1988). B. Eels All eel species spawn in sea water, in defined areas, and show a larval pelagic stage (leptocephals). The
151 European eel which will be taken as an example (see for review Dufour 1986; Brusl6 1989; Fontaine 1989; Lecomte-Finiger 1990), probably spawns in the Sargasso Sea. Then leptocephals are carried by marine currents to European coasts. After 1-2 years, when approaching the continental shelf, they metamorphose into glass eels, most of which will enter fresh water. Little is known about this metamorphosis. Eels live for 5-20 years in fresh water, where they eat and grow, before migrating to the Sargasso Sea, which indeed involves accommodation to sea water. As in the case of Salmo salar, the catadromous migration to the sea is preceded by programmed developmental changes, which one may call metamorphosis as it includes important morphological changes. As the eels turn from yellow to black and white, this metamorphosis is called silvering. Like smoltification, silvering includes a number of changes related to the environment i.e. a number of new adaptations. Some of them are concerned with osmoregulation and facilitate ulterior accommodation to sea water (Thompson and Sargent 1977); this process (an anticipatory adaptation) also leads to a maladaptation to fresh water which contributes to triggering the catadromous migration (M. Fontaine 1975). The endocrine control of silvering is not precisely known even though thyroid and interrenal hormones are probably involved (M. Fontaine 1975; Epstein et al. 1971). In the following discussion, the accent will be put on those characters of silver eels, that appear to be adaptations related to the necessity of specific environmental conditions for sexual development and reproduction. Silvering includes sexual development, the female gonadosomatic index (GSI) being increased 5 to 10 times. However silver eels are still very far from sexual maturity. The ovary for instance is blocked at the first stages of vitellogenesis and the female GSI is around 2 whereas we know that it attains around 30 or more in mature animals (M. Fontaine et al. 1964). If silver eels are prevented from migrating, no further sexual development occurs. This indicates that external factors encountered during migration are necessary for complete sexual development. Moreover we know that transfer to sea water has no effect whatever.
The spawning areas of all eel species appear to be located close to oceanic trenches and the few migrating fish which were captured were found in deep sea (some hundred meters) (references in Fontaine 1989). Also, one apparently maturing eel was photographed in the neighbourhood of Bermuda Islands, 2000 m deep (Robins et al. 1979). Such findings led us to the hypothesis that hydrostatic pressure could be one factor involved in the triggering of sexual development. To test this hypothesis female eels were placed in cages and immersed from an oceanographical ship in the northern Mediterranean Sea. In a first experiment immersion was carried out at 450 m for 3 months. Compared to controls, these animals showed slight but significant ovarian development and, notably, pituitary type II gonadotropin (GTH) level was increased 27 fold (Fontaine et al. 1985). Another experiment with immersion at 850 m deep for 3 months gave similar results (Fontaine et al. 1987). Deep sea conditions imply several environmental factors, two of which appear to prevail: obscurity and hydrostatic pressure. As we have found that obscurity does not affect the pituitary (GTH) levels (Dufour and Fontaine 1985) we suggest that hydrostatic pressure is an important factor in triggering the eel gonadotropic brain-pituitary axis. If high hydrostatic pressure is indeed necessary for sexual maturation of the eel, it would give a meaning to the oceanic migration, which is the only way to achieve exposure to such conditions. It is interesting to note that silvering includes changes which are adaptations to deep sea life, such as a new retinal pigment (Carlisle and Denton 1959) and complexification of the swimbladder red body (Kleckner and Kruger 1981). We postulate that eel reproduction has to occur in specific deep oceanic areas. We view eel migration as the necessary means to attain sexual maturation at these favourable sites and at an appropriate time. I shall briefly deal with our data in the neuroendocrinology of eel reproduction in this context. A dual hypothalamic blockage (lack of GnRH secretion and dopaminergic inhibition of gonadoliberin (GnRH) action) is responsible for the very low gonadotropic function in silver eels (Dufour et al.
152 DEVELOPMENTAL CLOCK
ENVIRONMENT
~,,.~
gene expression cell differentiation and modulation of cell activity
1
morphofunctional changes
PHYSIOLOGICAL CHALLENGE I
I
phofunctional changes, lulation of cell activity, gene expression, cell differentiation.
I
ACCOMMODATION
I
ADAPTATION Fig. 2. From adaptation to accommodation.
1988). Gonadal steroids are able to exert a positive retrocontrol on GTH synthesis, an effect which was demonstrated both on protein (Dufour et al. 1983) and on mRNA (Querat et al. 1991). They also increase GnRH concentration in brain and pituitary (Dufour et al. 1989, 1992). The ovaries are much more responsive to a gonadotropic stimulation in silver than in yellow eels (Lopez and Fontaine 1990). We interpret these physiological controls as secondary adaptations imposed by the obligatory environmental conditions of spawning. The blockage of gonadotropic function prevents precocious sexual maturation. Gonadal development during silvering makes subsequent rapid sexual maturation possible (when the blockage is released by environmental factors). Positive steroid retrocontrol amplifies this process.
Concluding remarks The diverse examples considered here lead us to view adaptations as those programmed developmental events, the results of which are concerned with adjustment to the environment. Thus controls of thyroid hormone production and receptors are likely to be important in the expression of adaptations as they are for other developmental events. Adaptations, and the timing of their expressions, were acquired by evolutionary processes including
variation and selection, about which we can only speculate. Some adaptations were acquired because they were favourable to survival; they allow accommodations to environmental changes, which tend to maintain a set point (e.g., euryhalinity). Other adaptations were acquired because they were favourable to growth and/or reproduction. They lead to changes in the set point which prepare for, and which can trigger, a move to a new environment which is propitious to growth (e.g., salmon smoltification) or reproduction (e.g., eel silvering). Although adaptation and accommodation are clearly different, they may involve common cellular mechanisms. For instance stimulation of hormone secretion or of gene expression may be part of both of them. Yet, the initial steps are different. An accommodation is triggered by an external, environmental change whereas an adaptation is triggered by an endogenous developmental clock. Thus, the chains of events (the details of which still have to be precised in most cases) are different (Fig. 2). Further progress in the identification, the analysis and the understanding of adaptations will require interdisciplinary research including comparative physiology, evolutionary biology, developmental biology and physiological genetics. Acknowledgements The author thanks S. Dufour, B. Demeneix, J. Leloup-Hatey and J. Leloup for helpful discus-
153 sions. He also thanks B. Demeneix for correcting the initial English text. He is grateful to F. Lieron, N. le Belle and B. Vidal for their help in preparing the manuscript.
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surge in metamorphosing flounder larvae. Gen. Comp. Endocrinol. 70: 158-163. Munck, A., Guyre, P.M. and Holbrook, N.J. 1984. Physiological function of glucocorticoids in stress and their relations to pharmacological actions. Endocrine Rev. 5: 24-44. Nishioka, R.S., Kelley, K.M. and Bern, H.A. 1988. Control of prolactin and growth hormone secretion in teleost fishes. Zool. Science 5: 267-280. Pickering, A.D. 1981. Introduction: the concept of biological stress. In Stress and Fish. pp. 1-9. Edited by A.D. Pickering. Academic Press, London. Pisam, M. and Rambourg, A. 1991. Mitochondria-rich cells in the gill epithelium of teleost fishes: an ultrastructural approach. Int. Rev. Cytol. 130: 191-231. Pisam, M., Prunet, P., Boeuf, G. and Rambourg, A. 1988. Ultrastructural features of chloride cells in the gill epithelium of the Atlantic salmon, Salmo salar, and their modifications during smoltification. Am. J. Anat. 183: 235-244. Prosser, C.L. 1973. Comparative Animal Physiology. W.B. Saunders, Philadelphia. Querat, B., Hardy, A. and Fontaine, Y.A. 1991. Regulation of the type II gonadotropin a and 3 subunit mRNAS by estradiol and testosterone in the European eel. J. Mol. Endocrinol. 7: 81-86. Robins, C.R., Cohen, D.M. and Robins, C.J. 1979. The eels, Anguilla and Histiobranchus, photographed on the floor of the deep Atlantic in the Bahamas. Bull. Mar. Sci. 29: 401-405. Selye, H. 1950. Stress and the general adaptation syndrome. Br. Med. J. 1: 1383-1392. Specker, J.L. 1988. Preadaptative role of thyroid hormones in larval and juvenile salmon: growth, the gut and evolutionary considerations. Am. Zool. 28: 337-349. Thompson, A.J. and Sargent, J.R. 1977. Changes in the levels of chloride cells and (Na+ +K+) dependent ATPase in the gills of yellow and silver eels adapting to sea water. J. Exp. Zool. 200: 33-40. Thorpe, J.E. 1987. Smolting versus residency: developmental conflict in salmonids. Am. Fish Soc. Symp. 1: 244-252.
Adaptations versus accommodations: some neuroendocrine aspects in teleost fish Y.-A. Fontaine Laboratoirede Physiologie ginirale et compare du Museum national d'Histoire naturelle; Unite' d'Endocrinologie compare associee au C.N.R.S. Paris,France
I. Ambiguities of adaptation Broadly speaking an adaptation is a favourable adjustment to the environment. It represents both a process and a result, which give rise to a first ambiguity. In biology, adaptation occurs in two very different situations. On the one hand, individuals adjust to changing environments using morphofunctional modifications which are often called "physiological adaptations". On the other hand, in the course of evolution, organisms acquire hereditary characters (adaptations) which are favourable - given the environment - for their survival and reproduction. These hereditary characters include physiological elements. This ambiguity reflects the independent developments of evolutionary biology and of physiology since Darwin (1859) and Cl. Bernard (1879). It raises - or should raise - a problem to comparative physiologists, i.e., those who take into account species diversity (Prosser 1973) and who take an interest in specific diversity of functions and their regulations. One may feel that to complain about the use of the same word - adaptation - in two different contexts is simply a semantic argument. But I would argue that this confusion hinders any attempt to compare the physiological adjustments involved in the two situations and, hence, to analyze their relationship. Here, I will reserve the use of the word adaptation to its evolutionary meaning, i.e., to the hereditary characters which favour the adjustment of one
species to its environment. As to the adjustments which occur throughout the life span of an organism in response to environmental changes, several items have been proposed, such as "acclimation", "acclimatization" (Prosser 1973). Here I will use "accommodation" (Cuenot 1925). Clearly, accommodations depend on adaptations; the ability to accommodate is itself an adaptation. In order to analyze more precisely the articulation between adaptations and accommodations (see Fig. 1) as well as the diversity of adaptations, we shall consider a few examples of physiological adjustments involving the neuroendocrine system in teleost fish.
II. Responses to environmental changes A. Stress syndrome Any environmental change is likely to evoke stress syndrome. This is an excellent example of the semantic problem and will be briefly considered here for this reason. Indeed, since Selye (1950), stress syndrome is known as the "general adaptation syndrome" (GAS) whereas, in the terminology used in this paper, the various reactions to aggressions are typical accommodations. In fish as in other vertebrates, stress syndrome includes several steps (Pickering 1981; Colombo et al. 1990). Catecholaminergic systems and the hypothalamus-pituitary-interrenal axis are the main agents of the primary alarm reaction, which may in-
148
Result
ADAPTATION (1) (hereditary character involved in adjustement to the environment)
Process
ADAPTATION (2)
ACCOMMODATION (not
hereditary)
ACCOMMODATION (occuring in response to environmental change)
(Time scale)
(Evolution)
(1) An adaptation includes both genomic characters from them. It conditions (-->) the accomodation.
(Life span)
and the phenotypic characters which directly derive
(2) The adaptation process raises a number of questions which will not be discussed here (see GOULD and LEWONTIN, 1979; LEVIN, 1982). Fig. 1. Diversity of the biological adjustments to the environment.
clude the participation of other hormones such as prolactin (Avella et al. 1991). Catecholamines and cortisol may elicit a great diversity of responses (Mazeaud and Mazeaud 1981). The favourable character of certain responses is questionable, as, for instance, osmoregulation is disturbed by stress. However most of them, concerned with metabolism as well as with respiratory and cardiovascular systems, are accommodations which can favour "fight or flight" and then help the fish to cope with environmental challenges. Miinck et al. (1984) have suggested that, in mammals, one function of the pituitary-adrenal activation may be to prevent an overshoot of the various defence mechanisms (Miinck et al. 1984). The existence of GAS in most vertebrates suggests that the adaptations which underly it were acquired early in vertebrate evolution. A first set could be concerned with the neuronal systems controlling adrenocorticotropin cells, catecholaminergic neurons and chromaffin cells. It is worth noting that in rainbow trout groups of cortisol "high responders" and "low responders" could be selected for breeding purposes (Pickering and Pottinger, in Colombo et al. 1990). Another set of adaptations is certainly concerned with the nature of catechola-
mine and cortisol targets. The expression, or a nonexpression, of receptor in a given tissue will qualify it, or not, as a hormonal target. This is a powerful potential process of adaptation as it may lead to important changes in the overall stress response. It is possible that specific differences in hormonal receptors present in adipose tissue could explain the old conflictory data on the lipase response to stress and hormones (Mazeaud and Mazeaud 1981). The identification of actual adaptations underlying GAS would need more comparative data on species differing in their stress response and their ecoethological habits.
B. Adjustment to salt water (1) Accommodations All events induced by salinity changes are accommodations. Let us consider, for instance, the transfer of a teleost fish from fresh water to salt water. Osmosis leads to water loss and ion invasion that the fish will oppose by increasing drinking and ion secretion through epithelia, mainly gills. The ion secretion is carried out in a special cell type, the chloride cells, where it is driven by NaK ATPase
149 (Foskett 1987). In fresh water two types of chloride cells ( and ) are present; upon transfer to salt water, a cells degenerate whereas the a cells undergo hypertrophy and a new type, the accessory cells, appear (see Pisam and Rambourg 1991). Many endocrine systems participate in the accommodation process as shown by various experimental approaches (measurement of plasma hormone level or secretion rate, study of hormone effects). Short and long term regulations have been described. Several hormones (angiotensin, catecholamines, somatostatin, urotensins, glucagon, vasoactive intestinal peptide) are involved in rapid regulation (see Foskett 1987). Only slow acting hormones (mainly cortisol, prolactin - PRL - growth hormone - GH - and triiodothyronine - T 3) will be considered here. Changes in the metabolism of these hormones occur after salt water transfer: increased cortisol production and plasma GH, decreased plasma PRL (see Hirano 1991), increased T3 utilisation and thyroxine (T4 ) deiodination into T3 (Lebel 1991). Accommodating effects of GH and cortisol have been demonstrated on survival, on ion exchanges or on Na+K + ATPase (e.g., Bolton et al. 1987; McCormick and Bern 1989; Boeuf et al. 1990; Madsen 1990). The effect of GH is at least partly mediated by T 3, probably due to stimulation of T4 deiodination (Lebel and Leloup 1992). The hormonal control of chloride cell changes is still to be defined even though effects of cortisol (e.g., Laurent and Perry 1990), GH (e.g., Madsen 1990) and PRL (e.g., Herndon et al. 1991) on morphology and number of chloride cells have been demonstrated. Foskett (1987) suggested that cortisol and GH stimulate the differentiation and the division of chloride cells, respectively, while PRL exerts a dedifferentiating effect. (2) Adaptations The salinity range in which a fish is able to accommodate depends on the species, from stenohaline to euryhaline ones. Even within euryhaline fish which can live in fresh or in sea water (SW) - the efficiency of euryhalinity is variable: some fish can only perform a progressive accommodation whereas others can survive direct transfer.
The different abilities to accommodate are due to different underlying adaptations which can occur at different sites (e.g., control of hormone secretion and properties of chloride cells). GH and PRL cells may be controlled not only by hypothalamic factors but also by other pituitary cells and directly by plasma osmolality (Nishioka et al. 1988). The sensitivity of these cells to plasma osmolality may be an adaptive character. In vitro, rainbow trout PRL cells appear less sensitive to medium osmolality than PRL cells from other, non-salmonids, euryhaline fish (Gonnet et al. 1988). The capacity to differentiate several types of chloride cells (see above) is certainly a major adaptation to euryhalinity. It would be interesting to know if this capacity involves endocrine components such as the presence of certain hormonal receptors in various types of chloride cells. A diversity of adaptations is probably involved in euryhalinity. The identification and understanding of these adaptations require more comparative data on species with different degrees of euryhalinity and different life strategies. This diversity of adaptations is likely to reflect the diversity of the evolutionary processes which gave rise to the present euryhaline species. It is interesting to examine the distribution of euryhaline species within teleost phylogeny (Lauder and Liem 1983). The great majority of euryhaline species are distributed in two rather distantly related groups. The first includes two closely related orders: Elopomorpha and Clupeomorpha in which are found the great migrators, such as Salmo salar, Anguilla sp., Alosa sp.. The second group includes two very closely related orders: Atherinomorpha and Percomorphawhich include a number of well known euryhaline species (Gillichthys, Gobius, Mugil, Platichthys, Tilapia). It can be postulated that euryhalinity was first acquired in populations which happened to live in estuarine zones, this adaptation being obviously favourable for their survival. Then a second step would have been to take advantage of it to use fresh and sea water to a much larger extent as it is the case in the present great amphihaline migrators. In salmonids and clupeids (to which belong Alosa sp.) this organization of the life cycle is somewhat flexible and wholly freshwater species also exist (Thorpe 1987; Hoar 1988).
150 III. Complex life strategies The species which will be considered here have acquired complex life strategies in the course of evolution. Their environmental requirements became different for different stages of the life span such as larval and adult forms or growth and reproduction. Before discussing the examples of salmonids and eels, I will briefly mention the obvious case of classical metamorphosis. Metamorphosis of flatfish (Paralichthys)for instance corresponds to a complete ecological change from a pelagic to a benthic life. Metamorphosis represents, at least partly, expression of adaptations to the new environment. As for amphibians, thyroid and interrenal hormones appear to be involved in flatfish metamorphosis (Miwa et al. 1988; de Jesus et al. 1990). A. Salmonids Salmonids, all of which spawn in fresh water, show a great diversity in their life strategies (Thorpe 1987) and in the efficiency of their euryhalinity (Hoar 1988). Typical migratory species, such as the Salmo salar,grow in fresh water, as parrs, for a few years and then migrate to the sea in defined areas where a second phase of growth occurs. After some years, fish accomplish a second migration back to the area where they were born; the sexual maturation occurs during the freshwater anadromous migration. When young salmons enter in sea water, they accommodate according to the general pattern which was previously described. However the process occurs more readily than in certain other euryhaline fish and even certain other salmonids because they have undergone a kind of metamorphosis called smoltification. Although external factors may modulate or synchronize the time of smoltification, this is clearly a programmed developmental event (M. Fontaine 1975; Hoar 1988; Boeuf 1992). This metamorphosis involves a diversity of changes, especially of adaptations (i.e., of changes concerned with the ability to adjust to the environment). Important osmoregulatory changes occur so that, contrarily to parrs, smolts may be transferred to sea water without problems. This is certainly related to the spectacular changes occurring at the level of
chloride cells where accessory cells appear (Pisam et al. 1988). As mentioned before, in most euryhaline fish this differentiation occurs as accommodation upon transfer to sea water and depends on hormones, mainly GH and cortisol. The differentiation of accessory cells during smoltification may also be secondary to increases in GH and cortisol (which have indeed been observed, see Dickhoff et al. 1990). In any case one can see here an interesting example where similar events have completely different triggers, either a developmental clock (adaptation) or an environmental change (accommodation). Smolts in fresh water acquire characters of sea water fish. For this reason smoltification has often been called a preadaptation (an ambiguous term because it is used in another meaning in evolutionary biology (Lewin 1982)); it is indeed an anticipatory adaptation (see M. Fontaine 1983, 1991). On another hand, osmoregulatory changes lead to a maladaptation to fresh water which together with other changes (e.g., behavioural) trigger the catadromous migration (see M. Fontaine 1975, 1983, 1991; Thorpe 1987; Hoar 1988; Boeuf 1992). One should not forget that smoltification includes a number of changes related to still other functions (e.g., diverse metabolisms, see M. Fontaine 1975; Hoar 1988; Specker 1988; Boeuf 1992). They prepare the fish to the migration. They can be considered as secondary adaptations to the optimal environmental conditions of growth such as they have been retained in the course of the evolution. Smoltification, like more classical metamorphosis, probably depends on thyroid and steroid hormones, the plasma levels of which increase during the parr to smolt transformation (see Specker 1988; Dickhoff et al. 1990; Boeuf 1992). In an interesting generalization, Specker (1988) suggested that a fundamental role of thyroid hormones would be to "preadapt" animals to exploit new food sources. Finally smoltification is a reversible adaptation. If smolts are kept in fresh water they lose their high capacity to accommodate to sea water (Hoar 1988). B. Eels All eel species spawn in sea water, in defined areas, and show a larval pelagic stage (leptocephals). The
151 European eel which will be taken as an example (see for review Dufour 1986; Brusl6 1989; Fontaine 1989; Lecomte-Finiger 1990), probably spawns in the Sargasso Sea. Then leptocephals are carried by marine currents to European coasts. After 1-2 years, when approaching the continental shelf, they metamorphose into glass eels, most of which will enter fresh water. Little is known about this metamorphosis. Eels live for 5-20 years in fresh water, where they eat and grow, before migrating to the Sargasso Sea, which indeed involves accommodation to sea water. As in the case of Salmo salar, the catadromous migration to the sea is preceded by programmed developmental changes, which one may call metamorphosis as it includes important morphological changes. As the eels turn from yellow to black and white, this metamorphosis is called silvering. Like smoltification, silvering includes a number of changes related to the environment i.e. a number of new adaptations. Some of them are concerned with osmoregulation and facilitate ulterior accommodation to sea water (Thompson and Sargent 1977); this process (an anticipatory adaptation) also leads to a maladaptation to fresh water which contributes to triggering the catadromous migration (M. Fontaine 1975). The endocrine control of silvering is not precisely known even though thyroid and interrenal hormones are probably involved (M. Fontaine 1975; Epstein et al. 1971). In the following discussion, the accent will be put on those characters of silver eels, that appear to be adaptations related to the necessity of specific environmental conditions for sexual development and reproduction. Silvering includes sexual development, the female gonadosomatic index (GSI) being increased 5 to 10 times. However silver eels are still very far from sexual maturity. The ovary for instance is blocked at the first stages of vitellogenesis and the female GSI is around 2 whereas we know that it attains around 30 or more in mature animals (M. Fontaine et al. 1964). If silver eels are prevented from migrating, no further sexual development occurs. This indicates that external factors encountered during migration are necessary for complete sexual development. Moreover we know that transfer to sea water has no effect whatever.
The spawning areas of all eel species appear to be located close to oceanic trenches and the few migrating fish which were captured were found in deep sea (some hundred meters) (references in Fontaine 1989). Also, one apparently maturing eel was photographed in the neighbourhood of Bermuda Islands, 2000 m deep (Robins et al. 1979). Such findings led us to the hypothesis that hydrostatic pressure could be one factor involved in the triggering of sexual development. To test this hypothesis female eels were placed in cages and immersed from an oceanographical ship in the northern Mediterranean Sea. In a first experiment immersion was carried out at 450 m for 3 months. Compared to controls, these animals showed slight but significant ovarian development and, notably, pituitary type II gonadotropin (GTH) level was increased 27 fold (Fontaine et al. 1985). Another experiment with immersion at 850 m deep for 3 months gave similar results (Fontaine et al. 1987). Deep sea conditions imply several environmental factors, two of which appear to prevail: obscurity and hydrostatic pressure. As we have found that obscurity does not affect the pituitary (GTH) levels (Dufour and Fontaine 1985) we suggest that hydrostatic pressure is an important factor in triggering the eel gonadotropic brain-pituitary axis. If high hydrostatic pressure is indeed necessary for sexual maturation of the eel, it would give a meaning to the oceanic migration, which is the only way to achieve exposure to such conditions. It is interesting to note that silvering includes changes which are adaptations to deep sea life, such as a new retinal pigment (Carlisle and Denton 1959) and complexification of the swimbladder red body (Kleckner and Kruger 1981). We postulate that eel reproduction has to occur in specific deep oceanic areas. We view eel migration as the necessary means to attain sexual maturation at these favourable sites and at an appropriate time. I shall briefly deal with our data in the neuroendocrinology of eel reproduction in this context. A dual hypothalamic blockage (lack of GnRH secretion and dopaminergic inhibition of gonadoliberin (GnRH) action) is responsible for the very low gonadotropic function in silver eels (Dufour et al.
152 DEVELOPMENTAL CLOCK
ENVIRONMENT
~,,.~
gene expression cell differentiation and modulation of cell activity
1
morphofunctional changes
PHYSIOLOGICAL CHALLENGE I
I
phofunctional changes, lulation of cell activity, gene expression, cell differentiation.
I
ACCOMMODATION
I
ADAPTATION Fig. 2. From adaptation to accommodation.
1988). Gonadal steroids are able to exert a positive retrocontrol on GTH synthesis, an effect which was demonstrated both on protein (Dufour et al. 1983) and on mRNA (Querat et al. 1991). They also increase GnRH concentration in brain and pituitary (Dufour et al. 1989, 1992). The ovaries are much more responsive to a gonadotropic stimulation in silver than in yellow eels (Lopez and Fontaine 1990). We interpret these physiological controls as secondary adaptations imposed by the obligatory environmental conditions of spawning. The blockage of gonadotropic function prevents precocious sexual maturation. Gonadal development during silvering makes subsequent rapid sexual maturation possible (when the blockage is released by environmental factors). Positive steroid retrocontrol amplifies this process.
Concluding remarks The diverse examples considered here lead us to view adaptations as those programmed developmental events, the results of which are concerned with adjustment to the environment. Thus controls of thyroid hormone production and receptors are likely to be important in the expression of adaptations as they are for other developmental events. Adaptations, and the timing of their expressions, were acquired by evolutionary processes including
variation and selection, about which we can only speculate. Some adaptations were acquired because they were favourable to survival; they allow accommodations to environmental changes, which tend to maintain a set point (e.g., euryhalinity). Other adaptations were acquired because they were favourable to growth and/or reproduction. They lead to changes in the set point which prepare for, and which can trigger, a move to a new environment which is propitious to growth (e.g., salmon smoltification) or reproduction (e.g., eel silvering). Although adaptation and accommodation are clearly different, they may involve common cellular mechanisms. For instance stimulation of hormone secretion or of gene expression may be part of both of them. Yet, the initial steps are different. An accommodation is triggered by an external, environmental change whereas an adaptation is triggered by an endogenous developmental clock. Thus, the chains of events (the details of which still have to be precised in most cases) are different (Fig. 2). Further progress in the identification, the analysis and the understanding of adaptations will require interdisciplinary research including comparative physiology, evolutionary biology, developmental biology and physiological genetics. Acknowledgements The author thanks S. Dufour, B. Demeneix, J. Leloup-Hatey and J. Leloup for helpful discus-
153 sions. He also thanks B. Demeneix for correcting the initial English text. He is grateful to F. Lieron, N. le Belle and B. Vidal for their help in preparing the manuscript.
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