Review
Perspectives on concordant and discordant relations between insulin-like growth factor 1 (IGF1) and growth in fishes

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Abstract

Many physiological processes are modulated by the endocrine system, including growth. Insulin-like growth factor 1 is one of the primary hormones involved in growth regulation in vertebrates, including fishes. Current work on IGF1 in fishes is driven both by a desire to better understand mechanisms of growth as well as to develop a reliable index of growth rate. A review of studies relating IGF1 to growth broadly reveals positive and significant relations between IGF1 and growth; however, relations found in individual studies range from no correlation to highly significant correlations. Potential sources for this variation include both biological and methodological issues and range from differences in how growth is defined (changes in length or weight), the duration of growth assessed (weeks to months) and how growth is calculated (total change, rate, percent change); yet, these methodological concerns cannot account for all the variation found. A further review of the literature reveals a number of physiological conditions and environmental factors that might influence IGF1 level and the subsequent relation of that IGF1 level to growth rate. The term concordance is introduced to categorize factors that influence IGF1 and growth in a similar fashion, such that positive and significant relations between IGF1 and growth are maintained even though the factor stimulates changes in IGF1 level. Conversely, the term discordance is introduced to categorize factors that stimulate changes in the relations between IGF1 and growth, such that IGF1 is not an efficacious index of growth for both pre and post-stimulus fish combined. IGF1 and growth relations generally remain concordant after changes in nutrition (consumption rate or diet). Differences in IGF1 level of juvenile, maturing male and maturing female fish are common and IGF1–growth relations appear discordant between these groups. Acute changes in temperature and salinity induce discordant relations between IGF1 and growth but acclimation to persistent differences in environmental condition generally result in concordant relations. Overall, by discriminating between fish of differing physiological status and discerning and categorizing differences among environments one may effectively use IGF1 as a growth index for fishes.

Research highlights

► A review of relations between IGF1 and growth in fishes was conducted. ► Nutritional changes generally did not affect concordance. ► Temperature and salinity affects were varied. ► Maturation and gender strongly affected concordance. ► Overall, for given set of conditions IGF1 and growth were positively correlated.

Introduction

Somatic growth is an integral biological process, intrinsically linked to larval, juvenile and sexual development. Measures of growth may serve as indicators of organismal fitness; related to an animal’s ability to acquire and assimilate feed, maintain homeostasis and regulate metabolism. There are a potentially remarkable number of applications for a reliable growth index in fishes; including, assessing growth-related recruitment variation, habitat quality, affects of environmental stressors and indexing the overall relative fitness of individuals and populations.

The endocrine system is a key regulator of physiological processes such as growth and an obvious subject for investigating the development of a growth index. A number of hormones are essential for stimulating and/or modulating growth and have been proposed as possible growth indices; including growth hormone, insulin, the insulin-like growth factors and thyroid hormones (MacKenzie et al., 1998, Pérez-Sánchez and Le Bail, 1999, Mommsen, 2001). Mechanistically, each of these hormones is required for increases in cell size and number. However, the kinetics of production, release and clearance of hormones can obscure cause and affect relations between measures of hormone abundance and the effects of that hormone. For instance, investigators of growth hormone affects in large mammals have developed a paradigm that requires obtaining plasma samples every 10 min over a 24 h cycle in order to adequately assess the amount of growth hormone released from the pituitary (Veldhuis et al., 2008). This is obviously an untenable approach for assessing growth in free-living fishes.

Insulin-like growth factor I (IGF1) possesses a number of characters that suggest plasma measures of IGF1 may represent an integrated index of the biological actions of the hormone. Unlike growth hormone or insulin, IGF1 is not stored and released in pulses; instead, evidence suggest that IGF1 is released constitutively as it is produced. In addition, clearance of IGF1 from the blood is retarded by the actions of a suite of IGF binding proteins (Degger et al., 1999, Degger et al., 2000, Degger et al., 2001, Kelley et al., 2002); again, a character that allows for a relatively constant level of IGF1 in the blood as compared to other hormones. Evidence of interest in generating a growth index in fishes, and that IGF1 may serve as such a growth index, is provided by several studies and reviews that suggest that IGF1 might be a useful growth index (Pérez-Sánchez and Le Bail, 1999, Beckman et al., 2004a, Dyer et al., 2004a, Picha et al., 2008a, Picha et al., 2008b). However, it is still unclear if IGF1 may serve as a growth index for all fish and in particular, it is uncertain how environmental variation may interfere with the use of IGF1 as a growth index.

Section snippets

The study of IGF1 in fishes

The study of IGF1 in fish was initiated by the discovery of IGF1-like affects by Komourdjian and Idler, 1978, Lindahl et al., 1985 and Duan and Inui, 1990a, Duan and Inui, 1990b. Subsequently, mammalian IGF1 was shown to have physiological affects in fish (Duan and Hirano, 1990, McCormick et al., 1992, Pérez-Sánchez et al., 1992), the IGF1 gene was cloned and sequenced in coho salmon (Cao et al., 1989, Duguay et al., 1992) and the 1st plasma measures of fish IGF1 were accomplished (Anderson et

The relation of IGF1 level to growth in fishes

Pérez-Sánchez et al. (1995) first explored the utility of IGF1 as an index of food consumption and growth, demonstrating that graded levels of feeding resulted in graded levels of IGF1. Subsequently, a significant and positive correlation between mean plasma IGF1 levels and mean growth rates of juvenile Chinook salmon was demonstrated (Beckman et al., 1998). However, other studies have found no relation between IGF1 and growth (Silverstein et al., 1998, Nankervis et al., 2000) leading to

Assessing IGF1 and growth: what is growth?

At its most basic level, growth is simply a change in size over time. The change in size of a fish over time may be assessed by measuring differences in length and or weight. Growth in length is a distinctly different physiological process from growth in weight and growth in weight itself may involve a number of physiologically distinct processes (muscle growth, liver growth, viscera growth, gonad growth and lipogenesis).

IGF1 clearly plays a role in growth of cartilage and bone tissue and

Assessing IGF1 and growth: What is the temporal span of a growth index?

Growth represents change in size over time. The temporal span of a growth measurement may vary from minutes to years. The shortest period over which a growth measurement may be made is determined by the actual growth rate of the fish and the precision with which one may measure size. The longest period over which one might measure growth is the lifespan of the fish, but at this scale measures of growth vary little from measures of size. Operationally, growth measures on the span of months to

Assessing IGF1 and growth: How is growth calculated?

Absolute size is an excellent measure of growth across the entire lifespan of an individual fish. For same-age fish, especially larval or juvenile fish, size may provide an adequate assessment of growth. In addition, growth (either length or weight) can be represented as a simple change: (measure2  measure1); as a rate: (measure2  measure1)/(day2  day1); or as a specific growth rate (SGR): (ln measure2  ln measure1)/(day2  day1) * 100. Jobling (1983) proposed a size independent measure of growth as

Assessing IGF1 and growth: snapshot vs longitudinal experimental design

Two fundamentally different experimental designs have been used to assess the relations between IGF1 and growth. The snapshot design is fairly straight-forward, all the fish are measured at the initiation of the study and all fish are measured and samples taken at the same time at the end of the growth stanza. In a longitudinal study growth rates and samples are obtained along a time course and growth rates and samples obtained at differing times are combined for analysis. Longitudinal sampling

Assessing IGF1 and growth: individual or mean values?

Various studies may assess the relation to IGF1 to growth through analysis of either individual fish values or mean values for groups of fish (treatments). These data assessments are not statistically equivalent as when means of groups of fish are correlated, all the variance associated with the mean (variation between individuals in the sample group) is lost. Generating mean values is much easier logistically as individual fish do not have to be marked and tracked. Many of the IGF1–growth

Assessing IGF1 and growth: are igf1 mRNA levels related to circulating plasma IGF1 levels?

IGF1 is produced in almost every tissue and has ubiquitous autocrine and paracrine actions on cells in all tissues. Endocrine IGF1 (circulating in the blood) comes mostly from the liver. IGF1 is a protein, production of the hormone is dependent on transcription of the IGF1 gene into mRNA and subsequent translation of the mRNA transcript into a protein. Thus, changes in igf1 mRNA level may correspond to changes in protein level. Distinct changes in hepatic igf1 mRNA level that correspond to

Assessing IGF1 and growth: conclusions

Results of experiments and studies assessing the relations of IGF1 to growth vary according to how growth was assessed (length or weight), how growth was calculated and experimental design (Table 1). These methodological issues may account for some differences in experimental findings. Even after accounting for these differences, significant variations in IGF1–growth relations are evident. The physiological status of the fish assessed and environmental factors used to modulate growth may also

Assessing physiological and environmental affects on IGF1 and growth: concordance

IGF1 levels might be influenced by many different environmental factors and physiological conditions, these interactions will form the focus for the rest of this review. However, it might be most informative if one examines how these environmental and physiological affects influence IGF1 level in relation to simultaneous changes in growth rate. For IGF1 to be an effective index of growth these same factors must affect growth rates and IGF1 in a concordant manner (Fig. 2), changes in IGF1 level

Assessing physiological and environmental affects on IGF1 and growth: acute vs persistent affects

One final consideration must be made before environmental and physiological effects on the relations between IGF1 and growth may be discussed. Changes in IGF1 level might be transitory and directly in response to a stimulus that has no affect on appetite, consumption or growth, or; changes in IGF1 level may take place over a longer period and represent changes due to differences in appetite, feed assimilation and metabolism and be directly related to changes in growth. Within the course of this

Environmental factors that affect IGF1 and growth: nutrition-consumption

Pérez-Sánchez et al. (1995) demonstrated that increasing the ration fed to gilt-head seabream (Sparus aurata) resulted in increased plasma IGF1 levels. Subsequently, numerous studies have shown that fasting reduces plasma IGF1 levels and these levels may be restored by re-feeding (Picha et al., 2008a, Picha et al., 2008b). Plasma IGF1 levels have been found to vary proportionally with increases and decreases in feeding rate (coho salmon Pierce et al., 2001a, Pierce et al., 2001b, Beckman et

Environmental factors that affect IGF1 and growth: nutrition-feeding/fasting time course

An important consideration for evaluating the IGF1 results is the time course of response to feeding and fasting. Pierce et al. (2005) measured daily (for 1 week) and then weekly (for six weeks) changes in plasma IGF1 and hepatic igf1 mRNA in juvenile Chinook salmon as they progressed through a fast. Significant differences in plasma IGF1 were not apparent until 4 days after the fast was initiated. Further decreases in plasma IGF1 level were apparent through 15 days of fasting, after which no

Environmental factors that affect IGF1 and growth: nutrition–diet

Historically, the aquaculture industry has used fish meals and fish oils as the basis for manufactured feed for cultured fish. The high cost of these products has resulted in substantial research activity directed at replacing fish based components of artificial feeds with other protein and oil sources (Gatlin et al., 2007). Some of these studies have used IGF1 as a marker for the efficacy of these formulations. There have been three main results of these studies (1) no difference in growth or

Physiological status and IGF1–growth relations

The physiological state of the fish itself may affect growth, IGF1 and the relations between growth and IGF1. In the human health field, measures of IGF1 level have proved to be useful in diagnosing and monitoring a number of health conditions (Juul, 2003). Clinicians have found that they must account for age, gender and body mass index (BMI) among other factors in order to interpret plasma IGF1 levels appropriately (Lukanova, 2004, Berrigan et al., 2009, Faupel-Badger et al., 2009). It is not

Physiological status that may alter IGF1–growth relations: diel cycles

There would be significant implications for interpreting experimental results if there were daily changes in IGF1 level induced by entrained feeding times, light–dark cycles, or any other biological rhythm (Boujard and Leatherland, 1992). Ayson and Takemura (2006) compared hepatic igf1 mRNA levels of three groups of three day fasted juvenile rabbitfish (Siganus guttaus) taken at 3 h intervals over a daily cycle exposed to three photoperiod treatments: light:dark, continuous light, constant dark.

Physiological status that may alter IGF1–growth relations: size

Major physiological changes occur as fish age and grow. Metabolic rates change, patterns of feed consumption and growth change and rates and efficiencies of feed utilization and nutrient deposition change (Paloheim and Dickie, 1966, Clarke and Johnston, 1999, Azevedo et al., 2004, Dumas et al., 2007, Wiff and Roa-Ureta, 2008). Size itself is not a physiological trait; however, differences in size provides a reliable index of differences in metabolic rate, maximum consumption rate (as a% of body

Physiological status that may alter IGF1–growth relations: compensatory growth

The phenomenon of compensatory growth has been of considerable interest in the fish research community (Ali et al., 2003). Simplistically, compensatory growth represents a period of enhanced growth (greater than normal) following a period of fasting. At times, compensatory growth has been characterized by periods of hyperphagia and enhanced feed conversion, processes that are obviously attractive to fish culturists (Skalski et al., 2005). Picha et al., 2006, Picha et al., 2008a, Picha et al.,

Physiological status that may alter IGF1–growth relations: smolting

Smolting is a developmental process that occurs in juvenile salmon that both allows and stimulates the fish to undertake a freshwater to seawater transition. It is a relatively specialized process, limited to salmonids and would not be of much interest in a general review except for the fact that many of the pioneering studies of IGF1 in fish have been conducted in juvenile salmonids (McCormick et al., 1991, Duan et al., 1995, Sakamoto et al., 1995, Moriyama et al., 1997). It is quite difficult

Physiological status that may alter IGF1–growth relations: gender and maturity

Sexual maturation requires shifting resources from maintaining and supporting somatic muscle growth to the stimulation and support of gonadal growth. These shifts are modulated through the endocrine system and involve both the GH-IGF1–growth axis and the gonadotropin–gonadal steroid axes. Steroids directly affect the patterns of GH release from the pituitary in mammals (Veldhuis et al., 2006) and androgen treatments stimulate both growth (Higgs et al., 1982) and IGF1 (Riley et al., 2002a, Riley

Juvenile and maturing fish

Moriyama et al. (1997) first demonstrated significantly increased plasma IGF1 levels in precociously maturing male salmon (O. masou) as compared to juvenile fish; subsequently, Campbell et al. (2003) and Larsen et al., 2004a, Larsen et al., 2004b Larsen et al., 2006, Larsen et al., 2010 have found significantly higher plasma IGF1 levels in maturing male Chinook salmon as compared to non-maturing fish of the same age class. In addition, Campbell et al. (2003) found a significant correlation

Maturing fish

Onuma et al. (2010) sampled maturing male and female chum salmon during their spawning migration from the Bering Sea, through near shore, estuarine and freshwater habitats of Hokkaido Island, Japan. Onuma et al. (2010) found significantly higher plasma IGF1 and hepatic igf1 mRNA levels in maturing male and female chum salmon caught at sea as compared to juveniles caught at sea. Both plasma IGFI level and hepatic igf1 mRNA level varied through the maturational period in males and females with

Gender

Differences in male and female size, growth and IGF1 levels have been found in tilapia. Riley et al. (2002a) showed significantly higher levels of both hepatic igf1 mRNA and plasma IGF1 occurred in male than female tilapia. Davis et al., 2008a, Davis et al., 2008b found significantly higher mean hepatic igf1 mRNA and plasma IGF1 level in male tilapia as compared to female tilapia and noted that male tilapia growth is generally higher than found in females. Similar to tilapia, Davis and Peterson

Genetics

Differences in gender represent a genetic difference between individuals. In addition, different strains, populations or species of fish may have differing genetic architectures that result in differences in the endocrine growth axis. For instance, GH treatment does not stimulate IGF1 levels in either yellow or Eurasian perch (Jentoft et al., 2004, Jentoft et al., 2005), suggesting IGF1 might be GH independent in these species. A number of studies have compared growth and IGF1 levels in

Physiological status that may alter IGF1–growth relations: stress

Simplistically, stress represents a disturbance that invokes a physiological response in fish. One of the most studied physiological responses to stress is an increase in the hormone cortisol and in many cases investigators have used the magnitude and duration of a cortisol elevation to define the stress response. A large literature exists on stress, stress affects, cortisol and cortisol affects in fishes (Barton, 2002, Mommsen et al., 1999, Bonga, 1997). In fish, the study of IGF1 response to

Physiological status that may alter IGF1–growth relations: disease

The potential for the initiation of discordant relations between IGF1 and growth in diseased fish is based on data demonstrating that GH stimulates immune response in fishes (Biga et al., 2005, Peterson et al., 2007, Yada, 2007). It is unknown how the stimulation of a GH-supported immune response might affect appetite, growth and the GH-stimulation of plasma IGF1 levels and the overall relation between IGF1 and growth. Bilodeau et al. (2006) found reduced mean plasma IGF1 levels in juvenile

Photoperiod: an environmental factor that alters the physiology of growth

The effects of photoperiod on growth and hormones are myriad (Boeuf and Le Bail, 1999), for the purposes of this discussion only one will be addressed: seasonal photoperiod change. Seasonal changes in photoperiod result in seasonal changes in appetite, feed conversion, hormone levels and growth rates (Marchant and Peter, 1986, Pérez-Sánchez et al., 1994, Forsberg, 1995, Beckman et al., 2000, Mingarro et al., 2002, Nordgarden et al., 2005). If increasing spring photoperiods result in an increase

Varying photoperiod, temperature and feeding rates

Taylor et al. (2005) compared growth and plasma IGF1 level of juvenile female rainbow trout exposed to one of three photoperiod regimes (a simulated natural photoperiod, constant short-day or constant long-day photoperiods) and sampled approximately monthly from June through December. Water temperatures ranged from ∼10 °C at the initiation of the experiment (June) to a peak of ∼16 °C in August and declined to 2 °C in January. Feed amounts varied with water temperature and fish size. Mean weights

Environmental factors that affect IGF1–growth: temperature

Temperature has strong direct and indirect affects on many physiological processes; including appetite, feed conversion efficiency and growth (Brett, 1979). As such, differing temperatures might be expected to result in differing IGF1 levels. The affects of acute temperature change have been examined in several species. Larsen et al. (2001) found significant decreases in plasma IGF1 levels three days after fish experienced at 10–2.5 °C temperature change, fish that were maintained at 10 °C and

Environmental factors that may affect IGF1–growth: salinity

Differing rearing salinities can directly affect potential growth rates in fishes (Boeuf and Payan, 2001). In addition, both GH and IGF1 have been implicated in the stimulation of hypo-osmoregulatory ability in fishes (Mancera and McCormick, 1998, Sakamoto and McCormick, 2006). Thus when investigating the effects of salinity on IGF1, one must consider that IGF1 level may respond directly to a salinity change because IGF1 has a role in modulating osmoregulatory abilities as well as a role in

Environmental factors that may affect IGF1–growth: toxicants

There are potentially a myriad of both short-term and long-term affects and interactions among water borne toxicants, appetite, growth and IGF1 levels in fish. Several studies have examined the effects of acute exposure to various toxicants on plasma IGF1 levels in smolting Atlantic salmon. Monette et al. (2008) found acid aluminum exposure reduced plasma IGF1 within 5 days as compared to controls in fasting fish, Lerner et al. (2007) found no affect of Arochor 1254 exposure on plasma IGF1 nor

Concordance and discordance between IGF1 levels and growth in fish and a prospectus for IGF1 as a growth index

In conclusion, plasma IGF levels appear to have many attributes that allow them to be used as a growth index; including a relatively high stability on the order of minutes to days and that changes in IGF1 level appear to accurately index changes in consumption (feeding/fasting and changes in feeding rate). However, to be a robust growth index, IGF1 levels must reflect growth under varying environmental conditions.

Study of the relations between growth and IGF1 level in fish in varying

Acknowledgments

My thanks to those who have made the NOAA laboratory at Montlake an exciting place to study the growth and endocrinology of salmonids, I’m quite fortunate to have been included in this group: Walt Dickhoff, Cunming Duan, Steve Duguay, Haru Fukada, Don Larsen, Adam Luckenbach, Shunsuke Moriyama, Andy Pierce, Erika Plisetskaya, Karl Shearer, Munetaka Shimizu, Jeff Silverstein, and Penny Swanson. In addition, I thank a number of current collaborators that are forcing me to think about how IGF1

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