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1 Minireview

2 Hormonal control of salt and water balance in vertebrates

3 Stephen D. McCormick a,b,¤, Don Bradshaw c
a
4 USGS, Conte Anadromous Fish Research Center, Turners Falls, MA, USA
b
5 Organismic and Evolutionary Biology Program, University of Massachusetts, Amherst, MA, USA
c
6 School of Animal Biology, The University of Western Australia, Perth, WA 6009, Australia

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7 Received 23 August 2005; revised 3 December 2005; accepted 13 December 2005
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9 Abstract

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10 The endocrine system mediates many of the physiological responses to the homeostatic and acclimation demands of salt and water
11 transport. Many of the hormones involved in the control of salt and water transport are common to all vertebrates, although their precise
12 function and target tissues have changed during evolution. Arginine vasopressin (vasotocin), angiotensin II, natriuretic peptides, vasoac-
13 tive intestinal peptide, urotensin II, insulin and non-genomic actions of corticosteroids are involved in acute (minutes and hours) altera-
14 tions in ion and water transport. This rapid alteration in transport is primarily the result changes in behavior, blood Xow to
D
15 osmoregulatory organs, and membrane insertion or activation (e.g., phosphorylation) of existing transport proteins, ion and water chan-
16 nels, contransporters and pumps. Corticosteroids (through genomic actions), prolactin, growth hormone, and insulin-like growth factor I
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17 primarily control long-term (several hours to days) changes in transport capacity that are the result of synthesis of new transport proteins,
18 cell proliferation, and diVerentiation. In addition to the important task of establishing broad evolutionary patterns in hormones involved
19 in ion regulation, comparative endocrinology can determine species and population level diVerences in signaling pathways that may be
20 critical for adaptation to extreme or rapidly changing environments.
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21  2006 Published by Elsevier Inc.

22 Keywords: Osmoregulation; Vertebrates; Ion transport; AVP; AVT; ANP; Angiotensin; Aldosterone; Cortisol; Growth hormone; Prolactin; IGF-I
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23 1. Physiological requirements for salt and water transport conserve water. The demands for ion and water transport 36
can vary greatly, depending on both internal factors such as 37
metabolic rate, and external factors such as salinity or 38
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24 Maintenance of constant intracellular and extracellular

25 ionic and osmotic environment (Bernard’s constancy of ‘le water availability. 39
26 milieu intérieur’) is critical for the normal functioning of Hormones play a critical role in signaling and control- 40
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27 cells. With several notable exceptions, such as hagWsh, ling the homeostatic and acclimation demands of salt and 41
28 sharks and ureotelic marine frogs, the majority of verte- water transport (Bentley, 1998). In spite of the diVerences in 42
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29 brates maintain a remarkably similar salt content of their transport needs and capabilities among vertebrates (and 43
30 extracellular Xuid, approximately one-third that of seawa- even the organs responsible for ion transport) many of the 44
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31 ter. This basic strategy results in diVerent transport hormones involved are remarkably similar. In addition to 45
32 demands for vertebrates depending on their external envi- acting on the basic mechanisms of ion transport, natural 46
33 ronment. In fresh water environments vertebrates must selection will act on the underlying neuroendocrine con- 47
34 actively take up salts, whereas in seawater they must secrete trols. Our understanding of large evolutionary trends (e.g., 48
35 excess salts. In terrestrial environments vertebrates must evolution of terrestriality) and adaptation of species to new 49
or severe environments requires knowledge of the underly- 50
ing control mechanisms for salt and water regulation. The 51
*
Corresponding author. Fax: +1 413 863 9810. purpose of this overview is to provide a general framework 52
E-mail address: mccormick@umext.umass.edu (S.D. McCormick). for the hormonal control of osmoregulation in vertebrates 53

0016-6480/$ - see front matter  2006 Published by Elsevier Inc.

doi:10.1016/j.ygcen.2005.12.009
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54 and to highlight the contributed papers to a symposium on classic example of an acute regulatory response is signaling 70
55 “Hormonal Control of Water and Salt Balance in Verte- by arginine vasotocin (AVT; or arginine vasopressin, AVP 71
56 brates” held in Boston in May 2005 as part of the Fifteenth in the case of mammals) to induce antidiuresis and thus 72
57 International Congress of Comparative Endocrinology. conserve water. Increased plasma osmolality (such as might 73
occur following reduced water intake or exposure to seawa- 74
58 2. Acute endocrine responses ter) signals osmosensors in the hypothalamus to release 75
AVT. Increased circulating AVT binds to membrane 76
59 Most organisms have at least a limited capacity to V2-type AVT receptors in the renal collecting duct, result- 77
60 respond to an osmotic or ionic challenge by rapidly chang- ing in the insertion of stored aquaporin (water channel) 78
61 ing existing transport mechanism. Some of these may be proteins into the plasma membrane. This increases water 79
62 independent of hormones (autoregulatory), such as changes reabsorption by the kidney permitting restoration of 80
63 in ion availability to transporters. Most changes in ion plasma osmolality. 81
64 transport, however, are cued by neuroendocrine or endo- Although it is likely that the AVT/AVP hormone has an 82
65 crine factors. Although there is a continuum of temporal osmoregulatory role in most vertebrates, the AVT–aquapo- 83

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66 responses, we can roughly divide transport responses into rin response may have evolved with terrestriality, since it 84

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67 those that activate existing transport mechanisms (acute has only been found to date in amphibians (Uchiyama and 85
68 regulatory response), and those that require development Konno, this volume) birds (Goldstein, this volume) and 86
69 of new proteins and cells (acclimation response) (Fig. 1). A mammals (Table 1). AVT functions as a physiological anti- 87

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diuretic hormone in the few species of reptiles that have 88
been studied to date and reduces glomerular Wltration rate 89

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ACCLIMATION PHASE
ACUTE PHASE and urine Xow by acting on both V1-type receptors in the 90
aVerent arteriole and V2-type receptors found in the thin 91
MC (genomic)
PLASMA HORMONE LEVEL

PROLACTIN intermediate segment and collecting ducts (Bradshaw and 92

GH / IGF-I
AVT/AVP
ANG II
Bradshaw, 1996). V2-type AVT receptors have also been 93
NAT PEPT
D
localized in the reptilian nephron (Bradshaw and Brad- 94
MC (non-genomic)
shaw, 2002). Shane et al. (2006, this volume) have shown 95
that AVT can stimulate amiloride-sensitive (ENaC) sodium 96
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reabsorption in the A6 Xenopus kidney cell line. Recent evi- 97

dence summarized by Balment (2006, this volume) indicates 98
that AVT is involved in salt secretion and/or water conser- 99
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vation necessary for seawater acclimation of teleost Wsh. 100

Although a V2-type AVT receptor has yet to be described in 101
)
)

Wsh, Perrott et al. (1993) have found that AVT can cause 102
ION / WATER TRANSPORT (
TRANSPORT CAPACITY (

increased cAMP in the trout renal tubules, consistent with a 103

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V2-type AVT receptor action in mammals. AVT at very low 104

doses is antidiuretic in Wsh (Balment et al., 1993), but AVT 105
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receptors are upregulated in sea water and localized in the 106

gill leaXets, suggesting a direct action of this peptide on the 107
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gills (Avella et al., 1999; Guibbolini et al., 1989). Thus, 108

AVT’s role in water conservation may have arisen early in 109
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MIN HOUR DAY WEEK vertebrates. It should be noted, however, that a wide diver- 110
sity of Wshes has yet to be examined. In particular it will be 111
OSMOTIC
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CHALLENGE of interest to determine if this response is present in teleosts 112

that are restricted to fresh water where demands for water 113
Fig. 1. Schematic diagram of the hormonal control of ion and water trans-
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port. Osmotic stimulus (such as alteration in internal osmotic pressure conservation may have placed little selection on develop- 114
caused by dehydration or exposure to seawater) results in release of rapid ment or maintenance of this capacity. Acher (2002) has sug- 115
acting hormones (blue) that activate existing proteins and cells to increase gested that “striking evolutionary stability” of AVT/AVP is 116
ion and/or water transport in the acute phase (seconds to hours) through the result of strong selection pressure on maintaining the 117
stimulation of existing mechanism (e.g., insertion of aquaporins into mem-
osmoregulatory function of this hormone. In contrast, the 118
branes or phosphorylation of transporters). Osmotic stimuli and rapid act-
ing hormones will increase long term acting hormones (green) to bring urea-based isosmotic strategy of cartilaginous Wshes has 119
about increased protein synthesis, cell proliferation, diVerentiation and tis- ‘released’ these Wsh from selective pressure allowing a 120
sue reorganization that will allow increased transport capacity in the accli- greater diversity of structure of AVT-like peptides in this 121
mation phase (several hours to several days). The ability to increase group of vertebrates. 122
maximum transport capacity will be present only in species with phenotypic
The natriuretic peptides, as their name implies, have 123
plasticity in response to osmotic challenge. Abbreviations: AVT D arginine
vasotocin; AVP D arginine vasopressin; ANG II D angiotensin II; NAT
important, acute osmoregulatory actions in vertebrates. 124
PEPT D natriuretic peptide; MC D mineralocorticoid; GH D growth hor- Since most vertebrates appear to have at least three forms 125
mone; IGF-I D insulin-like growth factor I. of natruretic peptides, generalization of their function must 126
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Table 1
Overview of major physiological function and target tissues (parentheses) of hormones critical to ion and water balance in vertebrates

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Elasmobranch Teleost Amphibian Reptile Bird Mammal
AVT/AVP Water retention Salt secretion ? Water retention Water retention Water retention Water retention

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#GFR "Cl secretion: G "absorption: K,S,UB "tubular reabsorption "tubular reabsorption "tubular reabsorption
#GFR #GFR #GFR

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Angiotensin II Water retention Water retention Water retention Water retention Water retention Water retention
"drinking "drinking "absorption: K "drinking "drinking "drinking
"aldosterone and cort

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"1a-hydroxycort "cortisol "aldosterone "aldosterone

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Natiuretic Pept Salt secretion Salt secretion Water and salt secretion ? Water and salt secretion Water and salt secretion

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"Na secretion: RG #drinking "GFR "GFR "GFR
#Na uptake:I #aldosterone #aldosterone* #aldosterone
"Na secretion:SG
Corticosteroid Salt secretion ? Salt secretion (? uptake) Salt retention Salt retention Salt retention Salt retention
"Na secretion: RG "Na secretion: G "Na aborption: S,I,UB "Na reabsorption:K,I,UB "Na reabsorption:K,I "Na reabsorption:

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"Na and water uptake:I K,I,UB,SG,MG
Prolactin ? Salt and water retention Salt and water retention ? “Milk” Production Milk production
#Na and water perm:G,I #Na and water perm:S "growth and secretion:CS "growth and secretion:MG

D
GH/IGF-I ? Salt secretion ? ? ? Salt and water retention
"Na secretion: G "Kidney growth
"gill MR cells "tubular Na reabsorption

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#GFR
VIP Salt secretion ? ? Salt secretion Salt secretion ?
"Na secretion:RG "Na secretion:SG "Na secretion:SG
K D kidney, I D intestine, UB D urinary bladder, S D skin, SG D sweat gland, MG D mammary gland; Ad D adrenal/interrenal; RG D rectal gland; MR-mitochondrion-rich; CS D crop sac;

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GFR D glomerular Wltration rate. Indication of physiological eVect of a hormone indicates that it is present in at least one species, but may not be present in all. See Bentley (1998) and text for references.

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increased aldosterone in response to ANP has been found in turkeys (see Toop and Donald, 2004).

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127 be done with some caution (Takei, 2001; Toop and Donald, porters increase over 1–14 days following exposure to sea- 182
128 2004). It appears that natriuretic peptides in mammals pri- water (Hiroi et al., 2005; McCormick, 2001), thereby 183
129 marily function to control blood volume. Donald and Tra- increasing the overall capacity of the tissue to secrete 184
130 janovska (2006, this volume) suggest that in amphibians, sodium and chloride. Cortisol upregulates these transport- 185
131 natriuretic peptides function primarily to protect the ani- ers in most euryhaline teleosts, and in several model eury- 186
132 mal from hypervolemia following periods of rapid rehydra- haline species there is an important interaction of cortisol 187
133 tion. This eVect is caused primarily by direct eVects on GFR with the growth hormone/insulin-like growth factor I axis 188
134 and indirect eVects on corticosteroid secretion. In contrast, to increase salt secretory capacity of the gill Sakamoto and 189
135 Tsukada and Takei (2006, this volume) provide evidence McCormick (2006, this volume). Prolactin plays a critical 190
136 that natriuretic peptides (speciWcally atrial natriuretic pep- role in acclimation of teleosts to fresh water, and acts 191
137 tide, ANP) have a primary role in ion regulation in eels antagonistically to the action of GH to promote seawater 192
138 (and perhaps in many teleosts), and are only secondarily tolerance. Although the function of cortisol in ion regula- 193
139 involved in volume regulation. They demonstrate that ANP tion has been primarily ascribed to regulating salt secretory 194
140 inhibits both drinking behavior in seawater (thereby limit- mechanisms, there is some evidence that cortisol also has a 195

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141 ing salt uptake) and intestinal absorption of Na+. role in maintaining transport proteins that are important 196

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142 In addition the rapid actions that can be brought about for ion uptake, including Na+/K+-ATPase (McCormick, 197
143 by insertion of existing proteins into membranes and con- 2001). 198
144 trol of blood Xow to osmoregulatory organs, hormonally In most terrestrial vertebrates aldosterone has a critical 199

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145 induced changes in behavior can have important osmoreg- role in regulating the long-term capacity for Na retention, 200
146 ulatory eVects. ANG II has widespread eVects on drinking primarily through increased synthesis of renal, urinary 201

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147 behavior among vertebrates, thus promoting water uptake bladder and skin transport proteins. Laverty et al. (2006, 202
148 (Table 1; Nishimura, 1987). An interesting exception is in this volume) review evidence for the role of aldosterone in 203
149 adult amphibians where angiontensis II does not promote mediating the increased Na+ transport capacity of the avian 204
150 drinking (these animals apparently do not drink) but does lower intestine following acclimation to a low salt diet. This 205
151 promote behavioral water uptake by increasing the water
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increased transport capacity is due to increased cell prolif- 206
152 absorption response, wherein the animals press a highly eration, tissue remodeling and increased expression of the 207
153 vascularized ventral skin patch into water or moist soil epithelial Na+ channel (ENaC). Shane et al. (2006, this vol- 208
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154 (Uchyama and Konno, this volume). Following the discov- ume) have shown that the capacity of aldosterone to 209
155 ery of an unusual form of angiontensin II in elasmobranchs increase apical ENaC expression and sodium reabsorption 210
156 (Takei et al., 1993), it has been found that angiontensin has is remarkably similar in kidney cell lines from amphibians 211
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157 an important role in drinking behavior and steroidogenesis and mammals. This classic genomic steroid action takes 212
158 is these basal vertebrates (Anderson et al., 2006, this vol- several hours, consistent with the synthesis of new proteins. 213
159 ume). There is also evidence for a more rapid, non-genomic 214
action of aldosterone, though the membrane receptor and 215
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160 3. Acclimation endocrine responses signal transduction for these rapid action are still unclear 216
(Losel et al., 2002). Agamid lizards have been shown to 217
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161 Acclimation responses increase the overall capacity of respond slowly but eVectively to changes in sodium status 218
162 an organism to perform a physiological function. The accli- by a combination of renal and post-renal modiWcations of 219
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163 mation response is similar or identical to phenotypic plas- the urine (Bradshaw, 1997). There is some evidence that 220
164 ticity; its presence or absence will often determine the corticosterone may function to reduce renal sodium reab- 221
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165 capacity of an animal to live in certain habitats and thus sorption in salt-loaded lizards, but aldosterone acts as a 222
166 determine the ecological limits of species’ distributions. A classical mineralocorticoid in the reptilian nephron, i.e., is 223
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167 classic example of acclimation in human physiology is the natriferic and kaliuretic (Bradshaw and Rice, 1981). 224
168 increased capacity for oxygen extraction after exposure to It has long been held that in teleost Wsh cortisol carries 225
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169 high altitudes. This occurs over a period of days to weeks out both glucocorticoid and mineralocorticoid function, as 226
170 and is the result of changes in hemoglobin content, number aldosterone is present only in very low concentrations in 227
171 of red blood cells, capillary growth, and lung capacity. teleost Wsh. Aldosterone is present in primitive sarco- 228
172 In teleost Wsh the acclimation responses of the gill, gut pterygii (coelocanths and lungWsh) (Bentley, 1998), and 229
173 and kidney are largely responsible for the capacity of tele- aldosterone may have evolved a mineralocorticoid function 230
174 ost Wsh to move between fresh water and seawater, termed in conjunction with the evolutionary movement of these 231
175 euryhalinity. In the gill one of the primary seawater accli- vertebrates to land. The recent Wndings that Wsh express a 232
176 mation responses is an increase in the number and size of receptor with high sequence similarity with the mammalian 233
177 salt secretory cells, termed “chloride cells” or “mitochon- mineralocorticoid receptor opens up the possibility of a 234
178 drion-rich cells.” These cells have high levels of Na+/K+- more complex regulation of ion transport in teleost Wsh 235
179 ATPase, Na+, K+, 2Cl¡ contransporter (NKCC) and the than previously appreciated Prunet et al. (2006, this vol- 236
180 CFTR apical chloride channel that are responsible for salt ume). This receptor may be involved in osmoregulation, 237
181 secretion by chloride cells. In most teleost Wsh these trans- and if so cortisol might be working through two receptors 238
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239 to bring about both glucocorticoid and mineralocorticoid 4. Summary and perspectives 296
240 actions, or a ‘missing’ corticosteroid such as deoxycorticos-
241 terone may be acting through this putative mineralocorti- In this review we have summarized the acute and accli- 297
242 coid receptor. mation endocrine responses that regulate physiological 298
243 Pickford and Phillips (1959) were the Wrst to demon- responses to osmotic challenges. Acute response are rapid 299
244 strate prolactin’s important role in ion uptake in teleost (seconds to hours) that are the result of activation of exist- 300
245 Wsh. Prolactin exerts primarily long-term eVects on mem- ing transport mechanisms. Examples of acute regulation 301
246 brane permeability and transport function of the gill, gut, include behavioral changes such as drinking, altered blood 302
247 and kidney (Hirano, 1986). Sakamoto and McCormick Xow, insertion of transporters into the plasma membrane, 303
248 (2006) propose that cell proliferation and diVerentiation are and phosphorylation of transporters. Acclimation 304
249 important mechanisms through which prolactin exerts responses occur over hours and days and are the result of 305
250 osmoregulatory actions in teleost Wsh. Prolactin also synthesis of new transporters (hours), cells (days) or even 306
251 reduces salt and water permeability in the skin of urodele tissue reorganization (several days to weeks). There is of 307
252 amphibians (Bentley, 1998). There is no apparent role of course a continuum and overlap in the time course of these 308

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253 prolactin in the overall salt and water metabolism in birds responses (Fig. 1) and the time course will diVer among spe- 309

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254 and mammals, although this hormone has osmoregulatory cies. There are also examples of intermediate types of 310
255 action in the sense of promoting Xuid production and secre- response, such as aldosterone’s induction of the small 311
256 tion in the crop sac of some birds and mammary glands of G-protein, K-Ras2, that activates ENaC and increases 312

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257 mammals. It is tempting to speculate that this ‘transfer of renal sodium reabsorption within hours Uchiyama and 313
258 function’ from whole animal osmoregulation to reproduc- Konnu (2006, this volume). While it is generally true that 314

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259 tion occurred in conjunction with the abandonment of peptides have rapid actions and steroids and large protein 315
260 freshwater during tetrapod evolution. With no selection hormones have longer-term actions, there are certainly 316
261 pressure to maintain its fresh water osmoregulatory func- exceptions; for example, aldosterone can have rapid, non- 317
262 tion, prolactin in terrestrial vertebrates may have been ‘free’ genomic action, and long-term remodeling can directly be
D 318
263 to adopt new functions. Since prolactin was already associ- controlled by peptides. 319
264 ated with the ‘water drive’ and fresh water spawning in There are important interactions among endocrine sys- 320
265 amphibians, it may have been predisposed to adopt a tems that allow the coordination of ion transport pro- 321
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266 reproductive function as tetrapods became wholly terres- cesses within and among tissues and across acute and 322
267 trial. acclimation phases. Hormones that are activated in the 323
268 As noted above, most teleosts upregulate gill chloride acute phase are often important signals for release of hor- 324
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269 (mitochondrion-rich) cells and their associated transporters mones in the acclimation phase. For example, angiotensin 325
270 in response to environmental salinity, and that this acclima- II and naturetic peptides cause opposite eVects on circu- 326
271 tion response is controlled by cortisol and the GH/IGF-I lating levels of aldosterone, and this regulation appears to 327
272 axis. In an analogous fashion, the salt gland of many birds be shared among many vertebrates. The ‘cross-talk’ 328
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273 can increase in size and Na+,K+-ATPase content in among hormones is clearly important in both Wne-tuning 329
274 response to environmental salinity (Skadhauge, 1981). and long-term adjustment of current transport and over- 330
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275 These salinity-induced changes apparently require an intact all transport capacity. 331
276 hypophysio-adrenocortical axis, though the role of cortico- We have emphasized the hormones that have a common 332
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277 steroids appears to be permissive. The size and Na+, osmoregulatory function among vertebrates (Table 1). 333
278 K+-ATPase activity of the NaCl secreting rectal gland of There are other hormones that have important functions in 334
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279 euryhaline elasmobranchs also varies in response to envi- ion and water balance that may be limited to a given phy- 335
280 ronmental salinity (Piermarini and Evans, 2000; Pillans lum, or whose role in osmoregulation has only recently 336
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281 et al., 2005). It would be of interest to determine if GH and/ come under investigation. Insulin stimulates ENaC-medi- 337
282 or IGF-I have a role in rectal and salt gland development ated Na+ transport in kidney tubule cell lines from both 338
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283 and diVerentiation that accompanies salinity acclimation of Amphibia and mammals (Shane et al., 2006, this volume). 339
284 elasmobranches and birds. To this end, preliminary studies Hughes et al. (2006, this volume) have found that melatonin 340
285 indicate that GH treatment can increase the relative size of increases the Na+ secretion of the salt gland of saline-accli- 341
286 rectal gland in hammerhead sharks (Björnsson, Sundell and mated gulls, and that salt acclimation increases melatonin 342
287 McCormick, unpublished results). GH and IGF-I have a receptors in the salt gland. Catecholamines by virtue of 343
288 clearly established role in repair of the kidney after tissue their dramatic vasoactive actions can have impacts on renal 344
289 damage and the compensatory renal hypertrophy that and gill Xuid homeostasis, and in teleost Wsh they also have 345
290 occurs after hemilateral nephrectomy (Rabkin and Schae- direct eVects on the function of chloride cells that are inde- 346
291 fer, 2004). In addition to these eVects on growth and diVer- pendent of their vascular eVects (Marshall, 2003). Uroten- 347
292 entiation, IGF-I may directly and indirectly (through sin II, originally thought to be restricted to Wsh, in now 348
293 stimulation of renin release and inhibition of atrial natri- known to be present in many vertebrates including mam- 349
294 uretic peptide) participate in glomerular and tubular mals and may have widespread eVects on Xuid and ion 350
295 sodium retention. homeostasis (Charrel et al., 2004). 351
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352 In outlining the broad evolutionary trends in hormone Guibbolini, M.E., Henderson, I.W., Mosley, W., Lahlou, B., 1989. Arginine 410
353 function (Table 1 and text), it is important to not that these vasotocin binding to isolated branchial cells of the eel: eVect of salinity. 411
J. Mol. Endocrinol. 1, 125–130. 412
354 represent the presence in a particular phylum, and that Hirano, T., 1986. The spectrum of prolactin action in teleosts. In: Ralph, 413
355 there are likely to be exceptions within any given phylum. C.L. (Ed.), Comparative Endocrinology: Developments and Direc- 414
356 Given the large number of species and diversity of habitats tions. A.R. Liss, New York, pp. 53–74. 415
357 to which some phyla have become adapted, the absence (or Hiroi, J., McCormick, S.D., Ohtani-Kaneko, R., Kaneko, T., 2005. Func- 416
358 addition) of a hormone function in some species or even tional classiWcation of mitochondrion-rich cells in euryhaline Mozam- 417
bique tilapia (Oreochromis mossambicus) embryos, by means of triple 418
359 whole clades is certainly possible. These may even be likely immunoXourescence staining for Na+/K+-ATPase, Na+/K+/2Cl¡ con- 419
360 where a phyletic group represents an altered habitat or life transporter and CFTR anion channel. J. Exp. Biol. 208, 2023–2036. 420
361 history with fundamentally diVerent osmotic challenges. Hughes, M.R., Kitamura, N., Poon, A.M.S., 2006. Osmoregulatory roles of 421
362 The coevolution of hormones and their receptors is an melatonin in birds with salt glands. Gen. Comp. Endocrinol. (this vol- 422
363 intriguing area that comparative endocrinologists are ume). 423
Laverty, G., Elbrond, V.S., Aranason, S.S., Skadhauge, E., 2006. Endocrine 424
364 uniquely positioned to investigate. As the major signaling regulation of ion transport in the avian lower intestine. Gen. Comp. 425
365 pathway for environmental osmotic stress, it seems likely

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Endocrinol. (this volume). 426
366 that the endocrine system will be a strong target of natural Losel, R., Feuring, M., Wehling, M., 2002. Non-genomic aldosterone 427

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367 selection when animals are in osmotically extreme environ- action: from the cell membrane to human physiology. J. Steroid Bio- 428
368 ments. This may result in diVerences in endocrine responses chem. Mol. Biol. 83, 167–171. 429
Marshall, W.S., 2003. Rapid regulation of NaCl secretion by estuarine tele- 430
369 and control among closely related species, and even result

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ost Wsh: coping strategies for short-duration freshwater exposures. Bio- 431
370 in intraspecies (population level) diVerences. Understand- chim. Biophys. Acta—Biomembranes 1618, 95–105. 432
371 ing both broad evolutionary and microevolutionary pat- McCormick, S.D., 2001. Endocrine control of osmoregulation in teleost 433

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372 terns will help establish the how evolution has shaped the Wsh. Am. Zool. 41, 781–794. 434
373 endocrine system and its control of osmoregulatory physi- Nishimura, H., 1987. Role of the renin–angiotensin system in osmoregula- 435
tion. In: Pang, P.K.T., Schreibman, M.P., Sawyer, W.H. (Eds.), Verte- 436
374 ology. brate Endocrinology: Fundamentals and Biomedical Implications, vol. 437
2. Academic Press, New York, pp. 157–187. 438
375 5. Uncited reference
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Perrott, MN., Sainsbury, R.J., Balment, R.J., 1993. Peptide hormone-stim- 439
ulated second messenger production in the teleostean nephron. Gen. 440
376 Goldstein (2006). Comp. Endocrinol. 89, 387–395. 441
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Pickford, G.E., Phillips, J.G., 1959. Prolactin, a factor promoting survival 442
of hypophysectomized killiWsh in freshwater. Science 130, 454–455. 443
377 References Piermarini, P.M., Evans, D.H., 2000. EVects of environmental salinity on 444
Na+/K+-ATPase in the gills and rectal gland of a euryhaline elasmo- 445
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