Hypotheses to explain

7.3.3 Hypotheses to explain

variability in strategies of the size and number of offspring

Various hypotheses have been proposed to explain variation in egg size and fecundity within and among species of fish. Many adaptive explanations centre upon proposed selection responses to species- and age-specific differences in the quality of parental care (Sargent et al. 1987) and to seasonal (Rijnsdorp and Vingerhoed 1994; Trippel 1998), population (Kaplan and Cooper 1984; Hutchings 1991, 1997) and individual (Jonsson et al. 1996) dif- ferences in access to food resources. Quinn et al. (1995) suggested that among-population variation in sockeye salmon, Oncorhynchus nerka, egg size can be explained as adaptive responses to differ- ences in the size composition of incubation gravel, arguing that the positive association between egg size and substrate size may be related to the latter’s influence on dissolved oxygen supplies relative to the surface-to-volume ratio constraints of eggs.

The reduction in egg mortality achieved by var- ious forms of parental care, expressed in the form of burying of eggs, predator defence, mouthbrood- ing and egg fanning, is considered a primary selec- tive factor responsible for the positive association between egg size and amount of parental care among species (Sargent et al. 1987; Forsgren et al., Chapter 10, this volume). Parental care may also offset the mortality costs associated with the longer developmental times of larger eggs. By ex- tension, the positive association between egg size and maternal size documented within many fish species has been attributed to a greater ability of larger females to provide parental care to their young (Sargent et al. 1987). Larger females may be able to provide greater protection to eggs. How- ever, the generality of this hypothesis must be tempered by the observation that egg size also increases with female size in fish that provide no parental care. This is shown by Atlantic cod (Chambers and Waiwood 1996; Kjesbu et al. 1996), Atlantic herring, Clupea harengus (Hempel and Blaxter 1967), caplin, Mallotus villosus (Chambers et al. 1989), and striped bass, Morone saxatilis (Zastrow et al. 1989).

Population differences in average egg size are often considered a proxy for adaptive variation. But, as previously noted elsewhere (Hutchings 1991; Reznick and Yang 1993), the relationship between offspring size and offspring survival must differ among environments, or among popu- lations, for environment- or population-specific egg-size optima to exist (Fig. 7.1). Hutchings (1991) reported the first such phenotype ¥ environment interaction on offspring survival in fish. Brook trout survival in the laboratory during the first 50 days following yolk-sac resorption was found to in- crease with egg size, but the effects of egg size and food abundance on juvenile survival were not addi- tive: decreased food abundance increased mor- tality among juveniles from the smallest eggs but had no effect on the survival of juveniles produced from the largest eggs, a finding similar to that observed for brown trout (Einum and Fleming 1999). Based on these experimental data, and sup- ported by field data on egg size and food abundance (Hutchings 1997), fitness functions described therefrom suggested that low food supply would favour the production of comparatively few, large offspring while high food abundance would favour females that produced many, comparatively small offspring (Hutchings 1991).

The dependence of environment-specific egg- size optima on the shape of the function relating offspring survival to egg size is illustrated in Fig.

7.1, where parental fitness (Fig. 7.1c,d) is approxi- mated by the product of egg survival and egg number, holding gonad volume constant. Two basic functions are considered: the size-dependent case, for which offspring survival varies continu- ously with egg size (Fig. 7.1a), and the size- independent case, for which survival above and below a very narrow range of egg sizes is constant (Fig. 7.1b). For the former, any factor such as food supply that is expected to increase offspring survival across all egg sizes is predicted to effect a reduction in optimal egg size (Fig. 7.1a), thus favouring females that produce relatively numer- ous, smaller offspring (Fig. 7.1c). By contrast, if offspring survival is independent of offspring size, optimal egg size is predicted to remain unchanged with changes in a factor that increases offspring

survival (Fig. 7.1d). Under such circumstances, the evolutionarily stable strategy of investment per offspring would appear to be one of maximizing the number of offspring, each approaching the physio- logically minimum size, within a brood.

Given the within-individual trade-off that must exist between egg size and egg number for a specific gonadal volume, it is evident that for selec- tion to favour an increase in egg size, the survival benefits to offspring produced from larger eggs must exceed the parental fitness cost of producing fewer eggs (Wootton 1994; Hutchings 1997). Un- fortunately, explicit recognition of this necessity is notably rare in many discussions of egg-size opti- ma, particularly in the marine fish literature. The fecundity cost associated with the production of large eggs must be acknowledged if natural varia- tion in egg size in fish is to be interpreted within an ecological or evolutionary framework. Demon- stration that larger eggs have lower predation or starvation mortality than smaller eggs need not in itself reveal anything about the selective advan- tage of producing large eggs or of the strength of a year-class composed of large eggs.

While the search for adaptive explanations for egg-size variability is perhaps more appealing in- tellectually, researchers need always be cognizant of the possibility that the observed variation has no adaptive basis. For example, egg size in many fish is negatively influenced by water tempera- ture (Pepin 1991; Kamler 1992; Chambers 1997). Trippel (1998) also cautions that seasonal declines in egg size in batch-spawning marine fish, such as Atlantic cod, might reflect a decline in the physio- logical condition of the female and a reduced abil- ity to allocate sufficient resources to each egg. It is also worth considering the high probability that a considerable amount of the variation in egg size, notably within females, is purely a function of de- velopmental noise or instability (Markow 1994). For example, among brook trout in Freshwater River, Newfoundland, for which the diameters of ten randomly chosen eggs were measured for each of 114 females (J.A. Hutchings, unpublished data), egg volume within females differed by an average 23%! Although one could argue that variable egg sizes within females in this case represents an

Life Histories

161

Chapter 7

adaptive response to unpredictable environmental exist within as well as between alternative heterogeneity (Kaplan and Cooper 1984), the hypo- strategies. thesis that this rather considerable amount of

Atlantic salmon males, a case in point, are typi- egg-size variability within females is a function of cally described as exhibiting alternative strategies developmental noise cannot be discounted.

(Myers 1986; Thorpe 1986; Hutchings and Myers 1988, 1994; Metcalfe 1998). Following a seaward migration as smolts, anadromous males return to

7.4 ALTERNATIVE LIFE-

their natal river and mature comparatively late

HISTORY STRATEGIES

in life (4–7 years) at a large size (45–90 cm). By contrast, mature male parr do not migrate to sea

Within populations, significant life-history varia- prior to reproduction, spawning relatively early in tion can exist among individuals of the same sex. A life (1–3 years) at a comparatively small size (<7– common observation is to find some males matur-

15 cm), whereafter they may or may not migrate ing relatively early in life, often at a comparatively to sea. Prior to spawning, dominant anadromous small size, attempting to obtain secondary access males defend access to an anadromous female to females by ‘sneaking’ fertilizations in competi- while mature male parr establish what appears to tion with later-maturing larger males who often

be a size-based dominance hierarchy immediately have primary access to a female through territorial downstream of the courting anadromous fish or mate-defence behaviours. Taborsky’s (1994) (Jones 1959; Myers and Hutchings 1987b). Mature review identifies 25 families (130 species) in male parr compete with one another and with which alternative reproductive strategies have anadromous males for the opportunity to fertilize been documented, the most common being the eggs (Hutchings and Myers 1988; Thomaz et al. labrids (e.g. Warner 1991), cichlids (e.g. Martin and 1997; Jones and Hutchings 2001, 2002). Taborsky 1997) and salmonids (e.g. Jones 1959;

However, it is not simply the gross differences Gross 1984; Thorpe 1986). A considerable litera- in body size and mating behaviour between ture exists on the terminology used to describe anadromous males and mature male parr that re- reproductive strategies and tactics (e.g. Taborsky quire explanation; age at maturity, body size and 1994; Gross 1996), much of which centres on the survival to maturity can differ significantly among degree to which the alternative life histories are of individuals adopting either the parr or anadro- genetic or environmental origin. For simplicity, mous male strategy (Myers et al. 1986; Hutchings and given that the relative contribution of genetic and Myers 1994). Thus, any evaluation of the and environmental factors to the expression of fitness associated with the mature parr and ana- alternative life histories is generally not known, I dromous male phenotypes will be incomplete use the term ‘alternative reproductive strategy’ without explicit consideration of the influence on to refer to the combination of life history and fitness arising from life-history differences within behavioural correlates of distinctive reproductive

each of these two strategies. Hutchings and Myers alternatives evident within a sex, within a single (1994) proposed a model to incorporate the exis- population, at one point in time (cf. Henson and tence of multiple age-specific sets of fitness func- Warner 1997).

tions within populations of Atlantic salmon. They

What precisely constitutes an ‘alternative re- suggested that the fitness of parr and anadromous productive strategy’? The phrase is often used males might best be represented as two multidi- somewhat loosely to describe usually two, occa- mensional fitness surfaces, and that the points of sionally three, sets of reproductive or mating be- intersection of these surfaces specified an evolu- haviours exhibited by members of the same sex tionarily stable continuum of strategy frequencies within a single population. However, by focusing along which the fitness associated with each solely on behaviour, one risks downplaying the ob- strategy would be equal. Approaching the same servation that significant life-history differences, question from a developmental perspective and

Life Histories

mate, influences on fitness, Thorpe et al. (1998)

High have developed a model that also incorporates fitness surfaces to explain life-history variation

High

within salmonids.