patterns in flies, fish, fruits and foliage - Wiley Online Library

241

Biol. Rev. (2007), 82, pp. 241–256. doi:10.1111/j.1469-185X.2007.00013.x

Ecological correlates of body size in relation to cell size and cell number: patterns in flies, fish, fruits and foliage Jeff Arendt* Department of Biology – Riverside, University of California, Riverside, CA 92521-6000, USA (Received 16 May 2006; revised 2 January 2007; accepted 3 January 2007)

ABSTRACT Body size is important to most aspects of biology and is also one of the most labile traits. Despite its importance we know remarkably little about the proximate (developmental) factors that determine body size under different circumstances. Here, I review what is known about how cell size and number contribute to phenetic and genetic variation in body size in Drosophila melanogaster, several fish, and fruits and leaves of some angiosperms. Variation in resources influences size primarily through changes in cell number while temperature acts through cell size. The difference in cellular mechanism may also explain the differences in growth trajectories resulting from food and temperature manipulations. There is, however, a poorly recognized interaction between food and temperature effects that needs further study. In addition, flies show a sexual dimorphism in temperature effects with the larger sex responding by changes in cell size and the smaller sex showing changes in both cell size and number. Leaf size is more variable than other organs, but there appears to be a consistent difference between how shade-tolerant and shade-intolerant species respond to light level. The former have larger leaves via cell size under shade, the latter via cell number in light conditions. Genetic differences, primarily from comparisons of D. melanogaster, show similar variation. Direct selection on body size alters cell number only, while temperature selection results in increased cell size and decreased cell number. Population comparisons along latitudinal clines show that larger flies have both larger cells and more cells. Use of these proximate patterns can give clues as to how selection acts in the wild. For example, the latitudinal pattern in D. melanogaster is usually assumed to be due to temperature, but the cellular pattern does not match that seen in laboratory selection at different temperatures. Key words: body size, cell size, cell number, resources, temperature. CONTENTS I. Introduction ...................................................................................................................................... (1) Background ................................................................................................................................. (2) Scope ........................................................................................................................................... (3) Comparing sizes .......................................................................................................................... II. Empirical examples ........................................................................................................................... (1) Arthropods – mostly Drosophila melanogaster ................................................................................ (2) Vertebrates – mostly fish ............................................................................................................ (3) Plants – fruits and foliage ........................................................................................................... III. Discussion .......................................................................................................................................... (1) General patterns ......................................................................................................................... (2) Additional patterns ..................................................................................................................... (3) Future directions ......................................................................................................................... IV. Conclusions ....................................................................................................................................... V. Acknowledgements ............................................................................................................................ VI. References .........................................................................................................................................

242 242 243 243 243 243 246 248 249 249 251 252 252 252 252

* Address for correspondence: E-mail: [email protected] Biological Reviews 82 (2007) 241–256 Ó 2007 The Author Journal compilation Ó 2007 Cambridge Philosophical Society

Jeff Arendt

242 I. INTRODUCTION

A

8

(1) Background Size

6

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0

m2

m1

2

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1

2

3

4

5

6

7

8

m1

m2

3

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5

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7

8

m2

m1

4

5

6

7

8

B

8

Size

6

4

2

0

1

0

2

C

8

6

Size

Body size is integral to most aspects of biology (Blanckenhorn, 2000) and is often the target of selection (Kingsolver & Pfennig, 2004). Fecundity generally increases with size (e.g. Stearns, 1992; Roff, 2002; Obeso, 2004) while competitive interactions (e.g. Werner, 1994; Schwinning and Weiner, 1998; French and Smith, 2005) and predator-prey interactions (e.g. Travis, Keen & Juilianna, 1985; Hoyle & Keast, 1987; Sogard, 1997; DeWitt, Robinson & Wilson, 2000; Downes, 2002) often depend on relative size. In addition, functional capabilities (e.g. locomotion) often scale with body size (e.g. Wilson & Franklin, 2000; Ojanfuren & Brana, 2003; Lovegrove, 2004) as do most physiological characteristics (e.g. Schmidt-Nielsen, 1983; Calder, 1984; Lovegrove, 2000). Size is probably the most commonly measured and manipulated character in biology. Despite its importance, we know remarkably little about how the developmental processes underlying growth relate to natural variation in body size. Several factors may influence size including differential allocation to organs or tissues (e.g. Calder, 1984; Zera, Sall & Grudzinski, 1997; Nijhout & Emlen, 1998) which in turn may depend upon cell number, cell size, extracellular matrix or any combination of the three. If body size is the variable of interest, why is it necessary to worry about the developmental processes that determine size? Many phenotypic manipulations alter size and age at maturation but different manipulations may arrive at this point via different trajectories (reviewed in Atkinson, 1994). For example, individuals reared at cool temperatures usually grow for a longer time and are larger and older at maturation than those reared at warm temperatures, resulting in crossing growth trajectories (Fig. 1A). By contrast, abundant food resources usually result in faster growth with earlier maturation at a larger size than low resource levels, resulting in nested growth trajectories (Fig. 1C). Clearly, what it means to be ‘‘bigger’’ is not the same in each context. The life-history consequences are fairly obvious. For crossing growth trajectories, rapid growth results in earlier maturation, but at the cost of a smaller size at maturation (Fig. 1A). The same trade-off may occur with nested trajectories (Fig. 1B), but often conditions that favour rapid growth result in both larger size and earlier age at maturation (Fig. 1C). These different trajectories are also likely to reflect different underlying developmental process. For example, a simulation model (Arendt, 2000) shows that changes in the patterns of cell recruitment can generate both crossing (via timing and rate of differentiation) and nested (changes in initial number of precursor cells) trajectories. However, this model did not include potential differences in rates of cell growth. There are also likely to be functional consequences of following one growth trajectory or another. For example, locomotor performance usually increases with size, but if different growth trajectories are the result of different underlying growth processes, then locomotion may scale with body size differently in each situation. If how a given body size is attained influences performance, then size alone

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Fig. 1. Relationships among growth trajectories can show three qualitatively different patterns. (A) If growth trajectories cross each other then faster growth results in a smaller ultimate size with earlier maturation, hatching, or metamorphosis (compare m1 and m2). This is a common pattern with temperature manipulations (Atkinson, 1994). (B) Nested growth trajectories mean that faster growers will always be larger than slow growers. In this case, faster growers may mature later (m2 in B) than slow growers (m1 in B), a pattern seen when comparing size and age at metamorphosis among species of spadefoot toads (Buchholz & Hayes, 2002). (C) Alternatively, faster growers may mature earlier than slow growers (m2 in C). This pattern is common in food manipulations, but is also how Orthoptera respond to temperature (Mousseau, 2000). Given the qualitative differences among these growth patterns, it seems likely they reflect distinct developmental processes.

Biological Reviews 82 (2007) 241–256 Ó 2007 The Author Journal compilation Ó 2007 Cambridge Philosophical Society

Ecological correlates of cell size and number is an inadequate predictor of performance. We may also need to pay attention to the underlying growth trajectories that determine body size in any study where size is important.

(2) Scope For this review I focus on how cell size and cell number contribute towards ecological variation in body size. This issue has usually been addressed from a bottom-up perspective, correlating genetic mutations with cell-cycle regulation and cell growth. There are several reviews covering genetic effects (Raff, 1996; Su & O’Farrell, 1998; Day & Lawrence, 2000; Hafen & Stocker, 2003; Kim & Sinha, 2003; Nijhout, 2003) which are useful in that they provide a mechanism for growth variation. However, this approach rarely relates variation to the environmental context within which size or growth plasticity evolve (Bochdanovits, van der Klis & De Jong, 2003 provide an important exception). In addition, many of these reviews seem to conclude that body size should be highly conserved because mutatations that change cell size are compensated by regulatory changes in cell number (and vice versa). This is clearly not the case as size varies widely depending upon rearing conditions and local adaptation. Here, I take a top-down approach and compare studies that identify how environmental variation in body size correlates with differences in cell size and number. It is my hope that once we know why particular groups of organisms differ in size (i.e. differences in cell size, cell number, or both) we can then proceed to determine the ecologically and evolutionarily relevant genetic mechanisms that determine these differences. For this review I have tried to include all relevant studies on multi-cellular plants and animals. Some study systems have been left out because they do not relate size to the environment (e.g. several studies have examined whether cell size or number correlate with different fruit sizes in agricultural strains, but it is not clear whether size variation was a result of artificial selection, local adaptation, or drift). Other studies are left out because they are of questionable generality. For example, because adults of the nematode Caenorhabditis elegans have a fixed cell number, body size can only vary by changes in cell size (Van Voorhies, 1996; Gumienny & Padgett, 2003). I also consider whether phenomena like crossed or nested growth trajectories are attributable to these cellular patterns. At this time we cannot make specific predictions about under which circumstances cell number should predominate and when cell size should predominate, or even if it matters. However, we can look for general patterns that will lead to more specific hypotheses. The questions I address here include: (1) does the same mechanism (cell size or number) correlate with differences in body size among different manipulations? (2) How general is a given correlation between a given mechanism and manipulation both within and among species? (3) Are environmental responses (i.e. phenotypic plasticity) similar to evolved (genetic) responses for the same manipulation? Finally, (4) can variation in mechanism explain differences in the shape of growth trajectories?

243 (3) Comparing sizes In looking for generalities among multicellular groups, we must first consider how to make comparisons across a diverse array of plants and animals. Longitudinal data (tracking individuals or populations throughout ontogeny) would be most useful for determining developmental patterns. For example, by surveying several species of freshwater fishes at multiple ages, Weatherley, Gill & Lobo (1988) were able to show that recruitment of new muscle fibres typically stops when fish reach approximately 44% of their asymptotic length with subsequent growth attributable to increase in cell size alone. Kundu, Patel & Mansuri (1994) found a similar pattern in a survey of seven species of marine fishes except that recruitment appears to stop at a larger proportion (51%) of asymptotic length. Longitudinal sampling can be used for organisms with indeterminate growth as easily as for those with determinate growth. The major disadvantage of longitudinal sampling is that it requires large sample sizes to sustain destructive sampling throughout ontogeny. Comparing populations or treatment groups by sampling at a single age is a simpler alternative. It seems logical that this single sample should be most informative after growth has stopped in organisms with determinate growth. Unfortunately, no equivalent time exists for organisms with indeterminate growth, making it impossible to compare determinate and indeterminate patterns. This problem can be alleviated if we focus on tissues or organs that show determinate growth even if the whole organism shows indeterminate growth. For example, although many plants have indeterminate growth, their leaves and fruits show determinate growth. In addition, a single sample after growth stops will necessarily confound size and age, although this should not be too serious an issue if one knows the shape of growth trajectories.

II. EMPIRICAL EXAMPLES (1) Arthropods – mostly Drosophila melanogaster The role of cell size and cell number in determining body size has been best studied in the epidermal wing cells of Drosophila melanogaster (Table 1). In D. melanogaster the plastic response to temperature results in crossing growth trajectories while the response to food results in nested trajectories. Early work suggested that temperature effects on adult size were due to changes in cell size, while the response to food level was due to cell number (Robertson, 1959). More extensive work with a number of D. melanogaster strains has largely confirmed the temperature response with an interesting sex difference. Both males and females show an increase in cell size with body size (i.e. when raised at lower temperatures), but males also show an increase in cell number that is absent in females. There has been only one additional study of food effects. De Moed, De Jong & Scharloo (1997a) manipulated both food and temperature and found an interaction between the two. At high temperatures cell number is the more important factor


Study

Species

Cell size

Cell number

Trajectory

Comments

Food plasticity

1 2

Drosophila melanogaster D. melanogaster

Temperature plasticity

1 3 4 5 6

D. D. D. D. D.

7

D. melanogaster

8

D. melanogaster

9

D. melanogaster

2

D. melanogaster

10 11

D. melanogaster dung fly Scathophaga stercoraria

12 3 6 5 13 14

cricket Allonemobius fasciatus D. melanogaster D. melanogaster D. melanogaster D. melanogaster D. melanogaster

5

D. melanogaster

0 0 ]] ]] ]] ]] ]] ]] ]] ]] ]] ]] ]] ]] ]] ]] ]] ]] ]] ]] [ ]] ]] ]] 0 0/[ ] ] 0/]

]] ]] ]] 0 0 0/] ] ] 0 ] 0 ] 0 ] 0 ] 0 0 0 ]] ]] 0/[ 0 [ ]] ]] ]] ]] ]]

nested ? nested crossing crossing crossing crossing crossing crossing crossing crossing crossing crossing crossing crossing crossing crossing crossing crossing crossing nested ? ? ? ? nested nested ? ?

15 4 7 16

D. D. D. D.

17

D. subobscura

12

A. fasciatus

] ] ] ] ]] 0 ] [

]] ]] ]] ]] ]] ]] 0 ]]

nested ? nested ? ? ? ? nested

at 25° C, female at 25° C, female at 15° C, female female female female (depends on food level) female male female male female male female male female male female sexes mixed male (confounded with food) female (confounded with food) warm larger female (depends on population) both sexes female both sexes larger (both sexes) smaller (both sexes) female (selection at 20° C) female (selection at 25° C, cell size only in small line) Australia Tanzania, France, Netherlands Australia Australia S. America S. America, Europe N. America low latitude larger

Selection on temperature Selection on humidity Selection on size

Latitudinal cline

melanogaster melanogaster melanogaster melanogaster melanogaster

melanogaster melanogaster melanogaster melanogaster

]] strong positive correlation, ] weak positive correlation. 0 no correlation, [ negative correlation.

Jeff Arendt

Comparison

244


Table 1. Correlations between body size and epidermal cell size or number in insects. Sources: (1) Robertson (1959); (2) DeMoed et al. (1997a); (3) Cavicchi et al. (1985); (4) De Moed et al. (1997b); (5) Noach et al. (1997); (6) Partridge et al. (1994a); (7) James et al. (1997); (8) French et al. (1998); (9) McCabe et al. (1997); (10) Azevedo et al. (2002); (11) Blanckenhorn & Llaurens (2005); (12) Mousseau (2000); (13) Kennington et al. (2003); (14) Partridge et al. (1999); (15) James et al. (1995); (16) Zwaan et al. (2000); (17) Calboli et al. (2003)

Ecological correlates of cell size and number underlying size differences in response to food, as Robertson (1959) found using similar conditions. However, at low temperatures cell size and number seem to play an equal role. Both studies used female flies; the pattern in males is not known. Studies using insects other than D. melanogaster are rare. Blanckenhorn & Llaurens (2005) report on a temperature manipulation in the dung fly Scathophaga stercoraria. Both sexes show a positive correlation between body size and epidermal cell size in the wing. As with D. melanogaster, cell number also plays a role in the smaller sex (male in D. melanogaster, female in S. stercoraria), but not the larger sex (although the sex X temperature interaction for cell number was not significant). Unfortunately, their results were confounded by a food manipulation that was not incorporated into the analysis. The plastic response in body size to food and temperature seem to be consistent although more work is clearly needed on the interaction between the two, especially in male flies. Do evolutionary changes in body size show any regular patterns for cell size or number? Laboratory adaptation following several generations of rearing at low temperatures results in larger flies. These flies are larger than warmadapted controls because they have larger cells (Cavicchi et al., 1985; Partridge et al., 1994a; Noach, De Jong & Scharloo, 1997), similar to the plastic response to temperature. However, the cold-adapted females also tend to have significantly fewer cells than do controls which is not seen in the plastic response; Partridge et al. (1994a) found no change in cell number for males, again in contrast to the plastic response. Finally, in a separate analysis Partridge et al. (1994b) show that the shape of growth trajectories for thermal adaptation follows a nested pattern rather than crossing as in the plastic response to temperature. Laboratory selection with humidity showed a pattern more like that seen with food manipulations in D. melanogaster (Kennington et al., 2003). Flies evolved to be larger at lower humidity, with size differences being driven entirely by cell number. In this case, sexes were distinguished but no difference was found. Artificial selection for body size shows a similar pattern, flies selected to be larger consistently have more cells than controls (Noach et al., 1997; Partridge et al., 1999). The importance of cell size was not consistent in these studies. Noach et al. (1997) found that if selection took place at 20° C then cell size played a small role in two of three comparisons. However, if selection took place at 25° C then cell size was important in only one of three comparisons, and then only in the line selected for small size. Partridge et al. (1999) conducted selection at 25° C and found that cell size was important but again only for the lines selected for small size. Only Partridge et al. (1999) reported growth trajectories which were nested. Because humidity and selection for large body size parallel the plastic response to food, it may be worth testing whether or not size differences are mediated by appetite and/or conversion efficiency (e.g. Bochdanovits & De Jong, 2003). A second approach to looking at genetic variation in body size is to compare populations along an environmental gradient. The only gradient to be studied extensively in D. melanogaster is latitudinal clines. When reared under

245 common conditions, flies from higher latitude populations are larger than those from lower latitudes (following Bergmann’s rule). This latitudinal cline in body size is generally interpreted as an adaptive response to temperature (James, Azevedo & Partridge, 1997; Zwaan et al., 2000) since temperature usually decreases as latitude increases and both artificial selection and rearing at low temperatures yield the same pattern. However, the contribution of cell size and number to body size differences does not match what we would expect from cold adaptation (fewer but larger cells) or temperature plasticity (similar cell number, but larger). Instead, when raised under common conditions high-latitude (larger) flies have more cells with little or no increase in cell size relative to low-latitude flies. The single exception I have found to this pattern is in D. subobscura, a fly native to Europe that was recently introduced to both North America and South America. In the European and South American populations larger flies have more cells of the same size, while in North America larger flies have larger cells but the same cell number as smaller flies (Calboli, Gilchrist & Partridge, 2003). Given the consistent difference in cellular composition it seems likely that the larger size of high-latitude flies is not directly due to temperature adaptation. Unfortunately, growth trajectories are not very useful in resolving this situation as no consistent correlation with nested or crossing trajectories has been found. James, Azevedo & Partridge (1995) show a negative correlation between development time and thorax length which means growth trajectories must be nested. James et al. (1997) found no correlation between latitude and development rate but since high latitude flies were significantly larger, growth trajectories must be nested. By contrast, Worthen (1996) found that high-latitude flies develop slower than-low latitude flies. Assuming high-latitude flies were larger, this would mean growth trajectories must be crossing. Latitude has a more consistent and dramatic impact on the length of the growing season than it does on temperature. Other organisms have evolved rapid growth and development rates in response to short growing seasons at high latitudes (e.g. Conover & Present, 1990; Margraf, Gotthard & Rahier, 2003; Bradshaw, Zani & Holzapfel, 2004; Gotthard, 2004). An alternative to temperature adaptation that may account for the cellular mechanism underlying body size in D. melanogaster is that a short growing season has selected for rapid growth via changes in feeding patterns and body size has simply shifted as a correlated response. For example, in Atlantic silverside (Menidia menidia) high-latitude fish have not altered temperature tolerance (Conover & Present, 1990), but show faster growth at a given temperature because of increased feeding rate and conversion efficiency (Present & Conover, 1992). Robinson & Partridge (2001) have also shown that D. melanogaster from high latitudes have greater conversion efficiency than those from low latitudes and Bochdanovits & De Jong (2003) showed flies from different latitudes differ in how they use glycogen. As others have suggested (Neat et al., 1995; James et al., 1997), latitudinal clines in D. melanogaster body size may not be a direct response to temperature but may reflect changes in resource use or competition (see also Santos, Brites & Laayouni, 2006).


Jeff Arendt

246 The only other arthropod to be examined for relative contribution of cell size and number to body size is the striped ground cricket (Allonemobius fasciatus). Crickets, and apparently all Orthoptera (Mousseau, 1997; Blanckenhorn & Demont, 2004), follow the converse of Bergmann’s rule. That is, animals from low latitudes are larger than those from high latitudes. In addition, crickets raised at cool temperatures are either similar in size (Roe, Clifford & Woodring, 1980) or smaller (Mousseau, 2000) at maturation than those raised at warmer temperatures (i.e. temperature results in nested rather than crossing growth trajectories). Both along a latitudinal cline and for crickets raised at different temperatures, the smaller crickets (from cold latitudes or rearing temperatures) have larger cells but fewer of them (Mousseau, 2000). We have no idea why crickets should follow such a different pattern from D. melanogaster, or even if the pattern is adaptive, but they are certainly not unique in the animal kingdom (e.g. Atkinson, 1995; Ashton & Feldman, 2003; Blanckenhorn & Demont, 2004). Van Voorhies (1996) has suggested that larger cells at cooler temperatures may be a general response in animals. If so, then the negative correlation between cell size and body size in crickets may be an unavoidable consequence of selection for large body size at warm temperatures or low latitudes. This is actually not a new idea and the pattern of larger cells at cool temperatures does not hold for many systems (reviewed in Atkinson, 1994) including muscle cells in fish (Section II.2), so if this constraint exists it must be more restricted than Van Voorhies (1996) originally suggested. In any case, it does appear that latitudinal clines in body size are driven primarily by cell number rather than cell size whether or not the species follows Bergmann’s rule. We can already begin to answer some of the questions posed in Section I. Clearly, different treatments generate variation in body size via different cellular mechanisms. In addition, the mechanism underlying the plastic response to rearing temperature is not identical to that underlying the genetic response to selection. Although both affect cell size, they have very different effects on cell number. A possible explanation may be that body size is not the actual target of selection in all cases, but that size may change as a correlated trait with another variable (e.g. age at maturation). Finally, where data are available, treatments that alter cell size generally produce crossing growth trajectories while those that influence cell number tend to produce nested trajectories. This contradicts the pattern predicted in the model of Arendt (2000), but that model did not allow for the possibility of differential cell growth. In addition, this pattern must be taken as preliminary as only a few species have been compared and the patterns are at best correlational. (2) Vertebrates – mostly fish Fish are the only vertebrate group that have been studied extensively with respect to the contribution of cell size and number to body size. The tissue examined has been the lateral muscle which can make up to 80% of the wet mass in fish (Weatherley & Gill, 1987). Cell recruitment can continue into adulthood in fish (Weatherley et al., 1988) making

interpretations of cell size and number patterns more difficult than in adult holometabolous insects where all cell growth and recruitment cease. Here, I report patterns for white (anaerobic) muscle fibres because these make up the bulk of the lateral muscles and studies do not consistently report on red (aerobic) fibres. Only a few studies investigated food effects on the cellular basis of growth in fish. As with D. melanogaster, increased food seems to accelerate growth by increasing cell number with little or no effect on cell size (Table 2). Fish fed more food are always larger than those fed less food resulting in nested growth trajectories. There do not appear to be any studies looking at the combined effects of food and temperature. Temperature effects present a more complicated picture. Many studies have only looked at embryonic growth, comparing fish at hatching. Because eggs incubated at cooler temperatures take longer to hatch, these fish are older and usually larger than hatchlings incubated in warmer water (i.e. equivalent to crossing trajectories). A number of studies with Atlantic salmon (Salmo salar) consistently find that coldincubated hatchlings have more but smaller muscle fibres than warm-incubated hatchlings. Work with herring (Clupea harengus) presents a very different pattern. All studies show that the larger fish have larger muscle fibres and when fish incubated at a cooler temperature were larger these hatchlings had fewer muscle fibres (the opposite of what was seen in Atlantic salmon). However, in one study (Johnston, 1993) the warm-incubated hatchlings were larger and size differences were determined by cell size. A later study (Johnston et al., 1998) found no size differences at hatching and no difference in muscle fibre size among temperature treatments (fibre number was not reported). The authors of these studies suggest that the inconsistency may reflect family differences; they have demonstrated family X temperature interactions in salmon (Johnston & McLay, 1997; Johnston et al., 2000b), and Johnston (1993) and Johnston et al. (1998) used eggs from only one and two females respectively. Johnston, Vieira & Abercromby (1995) used 20 families, perhaps removing this concern, and found herring to show the opposite pattern to Atlantic salmon. Embryonic growth in other species gives mixed results. As with herring, the larger fish at hatching (whether cold- or warm-treated) have larger muscle fibres but the effect on cell number varies (Table 2). The effects of temperature on larval and juvenile growth are much more consistent among species. In S. salar, C. harengus, and D. labrax the warm reared fish are larger at a given age and generally have both larger muscle fibres and more of them (Table 2). However, it is not clear how to relate these comparisons to those based on stage (e.g. hatching or metamorphosis). What can explain the diversity of patterns among species and among studies? Because of the early age at which fish have been sampled (rarely beyond larval metamorphosis), cell recruitment and cell growth are still occurring. Muscle fibre recruitment is not a continuous process; three phases of recruitment occur in fish (Johnston et al., 2000b; AlamiDurante et al., 2000), and this may obscure underlying patterns. In fish, the first fibres appear during somite formation in the embryo with separate cell lineages


Comparison

Study

Species

Cell size

Cell number

Trajectory

Comments

Food plasticity

1 2 3 4 5 6 7 8 9 10 11 12 13 14

cod Gadus morhua rainbow trout Oncorhyncus mykiss Atlantic salmon Salmo salar S. salar S. salar S. salar S. salar S. salar S. salar S. salar Atlantic herring Clupea harengus C. harengus C. harengus C. harengus

15 16

sea bass Dicentrarchus labrax D. labrax

17

D. labrax

18 19 20 21 22 23

D. labrax plaice Pleuronectes platessa G. morhua O. mykiss bleak Chalcaburnus chalcoides spotted turtle Clemmys guttata

0 0 0 [ [ [ [ [ [ ]/0 ]] ]] ]] 0 ]] ]] ]] ]] ]] 0 ]] 0 ] ]] ]] 0

]] ]] ]] ]] ]] ]] ]] ]] ]] ]/0 [ 0 [ 0 ]] ]] ]] ]] 0 ]] ]] [ [ ]] ]] 0

? nested nested crossing crossing crossing crossing crossing crossing nested crossing ? crossing nested nested nested nested nested ? nested nested crossing nested crossing nested ?

larval juvenile juvenile embryo embryo embryo embryo embryo embryo juvenile (depends on population) embryo embryo embryo embryo (no effects found) larval larval larval (48/55 days old) larval (at metamorphosis) embryo larval juvenile embryo embryo embryo embryo Cell number is negatively correlated with latitude, but not body size.


Latitudinal cline

Ecological correlates of cell size and number 247


Table 2. Correlations between body size and muscle fibre size or number for vertebrates. Symbols as in Table 1. Sources: (1) Galloway et al. (1999); (2) Rasmussen & Ostenfield (2000); (3) Johnston et al. (2002); (4) Stickland et al. (1988); (5) Usher et al. (1994); (6) Nathanailides et al. (1995); (7) Matschak et al. (1995); (8) Johnston & McLay (1997); (9) Johnston et al. (2000b); (10) Johnston et al. (2000a); (11) Vieira & Johnston (1992); (12) Johnston (1993); (13 Johnston et al. (1995); (14) Johnston et al. (1998); (15) Ayala et al. (2000); (16) Ayala et al. (2001); (17) Ayala et al. (2003); (18) Nathanailides et al. (1996); (19) Brooks & Johnston (1993); (20) Galloway et al. (1998); (21) Matschak et al. (1998); (22) Stoiber et al. (2002); (23) Litzgus et al. (2004)

Jeff Arendt

248 producing the slow red-fibres and fast white-fibres. The second phase of white fibre recruitment occurs along the dorsal and ventral edges (epaxial and hypaxial regions) of the main group of fibres; probably being derived from adjacent mesenchymal tissue. Fibres in the third phase of recruitment are derived from satellite cells located among the already existing muscle fibres. Species differ in the onset of each of these phases, and in some species the second (e.g. herring) or the third (e.g. guppies Poecilia reticulata) phase appear to be absent (reviewed in Alami-Durante et al., 2000). In addition, warm-reared animals initiate the second phase of recruitment earlier (Stoiber et al., 2002; Arendt, 2006). Given that cell size is usually measured as the average diameter of all cells in the muscle, and because newly recruited cells are small, rapid recruitment will tend to decrease the average fibre size even if there is no change in rate of fibre growth. Some authors recognize this potential bias and report cell size for only the largest few hundred fibres (those presumably recruited in the first phase). The effect of cell recruitment on average cell size may also explain why fibre recruitment is consistently faster for larval and juvenile comparisons, but fibre size is not. Taken together, these factors may also explain the differences in embryonic growth between Atlantic salmon and Atlantic herring. Because the second phase of recruitment begins before hatching in salmon, the older age of cold-incubated hatchlings includes a longer duration of recruitment. As a result, we would expect these fish to have more muscle cells at hatching. Herring skip the second phase and the third begins after hatching. If the first phase is relatively insensitive to temperature, then only cell size can respond to temperature. What of genetic differences in body size? No studies have examined cellular composition of fish along a latitudinal cline as in D. melanogaster. However, several papers report that populations may respond differently to the same temperature manipulation. Johnston et al. (2000a) compared a high-altitude (cold) breeding population of Atlantic salmon to a low-altitude (warm) breeding population and found that the former was largely unresponsive to temperature manipulation. Ayala et al. (2001) compared Mediterranean (probably warm water) to Atlantic (cold water) stocks of sea bass Dicentrarchus labrax. The former showed greater fibre growth when incubated at warmer temperatures while the latter showed no temperature effects in the embryo. However, Atlantic hatchlings did show faster fibre growth between hatch and first feed at warmer temperatures while the Mediterranean fish showed no response. Why Atlantic and Mediterranean stocks differ was not discussed. In both the salmon and sea bass examples, we do not know if population differences have any adaptive significance. Other vertebrate groups have not received much attention. Arendt (2006) found an interaction between food and temperature in the tail muscle of spadefoot toad Spea hammondii tadpoles largely due to the delayed second phase of recruitment at cool temperatures. Litzgus, DuRant & Mousseau (2004) compared the spotted turtle (Clemmys guttata) along a latitudinal cline. They found no clear association between body size and latitude or between direct measures of epidermal cell size and body size.

Estimates of cell density decreased significantly with latitude which might suggest an increase in cell size. However, direct measures of cell diameter were uncorrelated with latitude. The authors interpret their density estimates as evidence that interstitial space may be an important component of body size. These data are difficult to interpret because measures were made from turtles collected in the wild, thus confounding genetic differences with environmental differences along the cline. The pattern may indicate that no relationships exist, or that counter-gradient variation (see Conover & Schultz, 1995) obscures the pattern. Common garden studies will be needed to sort out these patterns. How do patterns observed for vertebrates compare to those for arthropods? As with D. melanogaster, food-level manipulations appear to alter size via changes in cell number. However, temperature manipulations do not show a consistent pattern in teleost studies. This may reflect real species differences not seen in arthropods because of the concentration of studies on D. melanogaster. In addition, most teleost studies investigated embryonic growth which may not be directly comparable to results from adult insects. What the teleost studies do show is that cell recruitment is not a simple linear process as described in most molecular reviews or models (e.g. Arendt, 2000); variation in cell number and size can be generated by varying the timing of different phases of cell recruitment. Serial sampling, rather than sampling at a single age or stage, will be needed to determine exactly how this translates into differences in body size. Imaginal discs in D. melanogaster also show multiple phases of cell recruitment (reviewed in Emlen & Allen, 2004), so this may be relevant to insects as well. (3) Plants – fruits and foliage Plants show a variety of growth forms. Many annuals, like Arabidopsis thaliana, have determinate growth such that vegetative growth stops at bolting. Although most plants have indeterminate growth, specific organs usually show determinate growth and studies of cell size and number have focused on two of these organs: fruits and leaves. All the studies I could find that investigated cell size and number were in angiosperms; primarily those of commercial importance. Because fruits compete for resources, fruit size is often negatively correlated with fruit number on a single plant. In addition, fruits that develop first on growing tendrils have a competitive advantage. Size variation due to competition among fruits acts primarily through cell number with less variation in cell size (Table 3). Some of the exceptions to this pattern have confounding factors: e.g. in Atkinson, Taylor & Kingswell (2001) differences in fruit number on a plant were due to plants being reared at different temperatures. Temperature influences cell number in cucumber Cucumis sativus (Marcelis & Hofman-Eijer, 1993) but there is also a consistent difference in cell size not seen in other fruits. The general influence of cell number during competition is similar to the effects of food in both insects and fish. Curiously, competition does not appear to be a simple result of carbohydrate availability as light and defoliation treatments alter cell size as well as number. Temperature effects on fruit also parallel those seen in animals. In a study on cucumber,


Ecological correlates of cell size and number

249

Table 3. Correlations between fruit size and cell size or number. Symbols as in Table 1. Sources: (1) Bohner & Bangerth (1988); (2) Bertin et al. (2003); (3) Bertin (2005); (4) Denne (1960); (5) Westwood et al. (1967); (6) Quinlan & Preston (1968); (7) Goffinet et al. (1995); (8) Atkinson et al. (2001); (9) Marcelis (1993); (10) Marcelis & Hofman-Eijer (1993); (11) Jackson et al. (1977) Comparison Competition plasticity

Study

Species

Cell size

Cell number

Trajectory

Comments

1 2 3

tomato Lycopersicon esculentum L. esculentum L. esculentum

4 5

apple Malus domestica M. domestica M. domestica M. domestica M. domestica M. domestica

0 0 0 ]] ] [ ] 0 0 ]]

]] ]] ]] 0 ]] ]] ] ]] ]] 0

nested nested nested nested nested ? ? nested ? ?

9 10 12

cucumber Cucumis sativus C. sativus M. domestica

]] ]] 0

]] 0 ]]

nested ? nested

1 9 3 10

L. esculentum C. sativus L. esculentum C. sativus

8

M. domestica

] ] [ ]] 0 ]]

]] 0 ]] 0 ]] 0

nested ? crossing nested crossing nested

position position position thinning thinning thinning thinning thinning thinning fruit number (confounded with temp) thinning thinning (depends on temp) light (confounded with fruit set) defoliation defoliation cold large (NS) 1 fruit on plant 5 fruits on plant confound w/ fruit set

6 7 8

Light level plasticity


when there is no competition among fruits, larger fruit size is determined by cell size alone. However, cell number is more important in determining fruit size when several fruits are present (Marcelis & Hofman-Eijer, 1993), an interaction similar to that seen in D. melanogaster (De Moed et al., 1997a). Leaf growth shows a less consistent pattern. In general, addition of nutrients (either nitrogen or phosphorus) results in larger leaves due to an increase in both cell size and number (Table 4). The one exception (Cruz, Lips & Martins-Loucao, 1997) compared source of nitrogen (nitrate versus ammonia) rather than total available nitrogen. Light effects are especially difficult to interpret because some species have larger leaves under high light conditions (e.g. cucumber) while others have larger leaves under low light (e.g. sweet pepper Capsicum annuum). These differences in plasticity may represent ecological adaptations with shade-tolerant species producing leaves of greater surface area in low light (e.g. McClendon & McMillen, 1982; Smith, 1991). Epidermal cell number plays a larger role for shade-intolerant species (cucumber and sunflower Helianthus annus) with epidermal cell size changes involved for shadetolerant species. Part of this variation among species may reflect the experimental light levels. For example, in the broad bean Vicia faba only cell number contributes to variation in leaf size at very low light levels, only cell size features at high light levels and both contribute to size changes at intermediate levels (Butler, 1963). Given the general importance of leaf size for shade tolerance (Dengler, 1994), much could be gained by examining underlying leaf growth patterns with reference to this ecological variable. Temperature effects on leaf growth are inconsistent. Tomato Lycopersicon esculentum leaves show a consistent

increase in size with temperature due to increased cell number. Wheat Triticum aestivum and bean Phaseolus vulgaris, on the other hand, show an increase largely due to cell size. Some studies used manipulations that are difficult to interpret: Milligan & Dale (1988) only manipulated root temperature and Auld, Dennett & Elston (1978) applied temperature manipulations late in leaf development, probably after most cell division had ended. Comparisons of fruit size among genotypes have been conducted for many agricultural varieties (e.g. Scorza et al., 1991; Cheng & Breen, 1992; Cong, Liu & Tanksley, 2002; Bertin et al., 2003). I have not found any studies looking at adaptation along an ecological gradient, although plants are known to show such growth and size clines (e.g. Li, Suzuki & Hara, 1998). How do patterns in fruits and leaves compare with animal systems? They are much less consistent for any given treatment. I suspect this is because many more species have been studied but with little replication within a species. In addition, most species studied are domesticated varieties usually selected for rapid growth or large fruits. This is likely to complicate interpretation of ecologically relevant patterns, making it hard to generalize.

III. DISCUSSION (1) General patterns Previous reviews have concluded that cell number is the most important factor determining organ and body size (Stevenson, Hill & Bryant, 1995; see also Humphries &


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250

Table 4. Correlations between leaf size and cell size or number. Symbols as in Table 1. Sources: (1) Roggatz et al. (1999); (2) Trapani et al. (1999); (3) Walter et al. (2003); (4) Cruz et al. (1997); (5) Hart & Collier (1994); (6) Milligan & Dale (1988); (7) Milthorpe & Newton (1963); (8) Isanogle (1944); (9) Butler (1963); (10) Wilson (1966); (11) Dengler (1980); (12) Granier and Tardieu (1999); (13) Granier et al. (2000); (14) Slade (1970); (15) Friend & Pomeroy (1970); (16) Rahim & Fordham (1991) (17) Schoch (1972); (18) Paul (1984); (19) Hoek et al. (1993); (20) Auld et al. (1978) Comparison Nutrient plasticity

Light level plasticity


Study 1 2 3 4 5 6 7 8 9 7 10 11 12 13 14 15 16 17 18 19 20 6 15

Species

Cell size

Cell number

Trajectory

Comments

castor bean Ricinus communis sunflower Helianthus annus tobacco Nicotiana tobacum carob (Ceratonia siliqua) clover (Trifolium repens) lotus (Lotus repens) bean (Phaseolus vulgaris) cucumber (Cucumis sativus) Norway maple Acer platanoides broad bean Vicia faba C. sativus C. sativus sunflower H. annus H. annus N. tobacum grass Poa alpina wheat Triticum aestivum garlic Allium sativum sweet pepper Capsicum annuum tomato Lycopersicon esculentum L. esculentum V. faba P. vulgaris T. aestivum

]] ]] ]] [ ]] ]] ]] ]] ]] ]]/] 0 0 0 0 0 ]] ]] ]] 0 0 [ ]] ]] ]]

] ]] ] ]] ? ? 0 ]] ] ]/]] ]] ]] ]] ]] ]] 0 ]] 0 ]] ]] ]] ] 0 ]/-

nested nested nested ? nested nested ? ? ? ? nested nested nested nested nested ? ? crossing ? nested nested crossing ? ?

nitrogen nitrogen nitrogen NO3 vs. NH4 phosphorus phosphorus root pruning pot size light larger light larger light larger light larger light larger light larger light larger shade wider shade larger shade larger shade larger warm larger warm larger warm larger (treatment late) just cooled roots hump-shaped reaction norm

Wheeler, 1963, and Coombe, 1976). Although cell number is obviously important in large-scale allometric comparisons (e.g. mouse to elephant), the same is not true for intraspecific comparisons. In their analysis of Hawaiian Drosophila species, Stevenson et al. (1995) emphasized the importance of both cell size and cell number, and the intraspecific comparisons described herein make it clear that both characters must be considered if we are to understand regulation of body size. A parallel conclusion is that different environmental factors influence body size through different mechanisms: even if two individuals are similar in size, they may have different cellular compositions reflecting the environmental conditions during either development or evolutionary history. Can we answer the questions posed earlier? Do the same cellular mechanisms explain differences in growth rate among treatments, and are these consistent among species? The answer to the first question is clearly no, and to the second a qualified yes. Different experimental manipulations result in variation in body size via different cellular mechanisms. Nutrient levels influence body or organ size predominately through changes in cell number, apparently across a variety of multi-cellular organisms, except in angiosperm leaves where cell size is equally or more important. Temperature effects are largely due to variation in cell size for D. melanogaster, several fruits, and leaves (although tomato plants appear to be an exception). The different responses in fish to temperature manipulation may

be due to the early developmental stage at which comparisons were made. Different growth processes may predominate at different ages (e.g. Atchley, Wei & Crenshaw, 2000) and thus variation in embryonic growth may not be directly comparable to variation in adult size. Third, how does developmental plasticity compare with evolved responses? As with environmental manipulations, selection experiments on D. melanogaster alter body size via different mechanisms. Especially curious is the fact that selection at cool temperature leads to a decrease in cell number compared with controls while simply rearing flies at cooler temperatures has either no effect (in females) or increases (in males) cell number. Thus although the phenotypic response and the evolved response to temperature both result in larger body size at cool temperatures, they do so in different ways. In addition, although latitudinal clines in D. melanogaster body size have usually been attributed to temperature adaptation, population comparisons do not match either the plastic response or the effects of temperature selection in the laboratory. Larger flies usually have more cells with increased cell size being minor in latitudinal comparisons while the increase in body size in response to cooler temperatures is mediated primarily through cell size. This difference suggests that latitudinal clines in D. melanogaster body size may represent adaptation to some other factor in addition to or instead of temperature. Comparisons of different populations of plants and vertebrates across environmental gradients are clearly needed.


Ecological correlates of cell size and number Fourth, can differences in cellular mechanisms explain differences in growth trajectories (crossing versus nested)? The best data exist for D. melanogaster: nested trajectories tend to be associated with differences in cell number while crossing trajectories more often are associated with cell size. For fish, temperature manipulations result in crossing trajectories via cell number for Atlantic salmon, so the pattern seen in D. melanogaster may not be universal. However, as noted above, it may not be appropriate to compare embryonic growth with juvenile growth especially as crossing trajectories may appear to be nested if comparisons are made early in development. For fruits and leaves, cell number is appears to be important when growth trajectories are nested but there are too few examples of crossing growth trajectories to draw any strong conclusions. However, light level seems to affect leaf size in a manner similar to the D. melanogaster pattern. Shade-tolerant species show crossing trajectories with cell size being most important in determining leaf size, while shade-intolerant species have nested growth trajectories with cell number being most important. Overall, the available data do not allow any strong conclusions to be drawn regarding the cellular mechanisms driving differences in growth trajectories. (2) Additional patterns Several interesting new observations emerge from these comparisons. First, there is an interaction between food and temperature in D. melanogaster, tadpoles and cucumber fruits, which should be explored further because growth under natural conditions is likely to reflect simultaneous effects of food and temperature. For example James et al. (1997) found that field-caught D. melanogaster along a latitudinal cline in Australia were always smaller than laboratory-reared flies from the same latitude; variation in size was due primarily to cell number, a pattern we expect from resource level, not temperature. They suggested that this pattern indicates flies are typically food limited in the wild. Secondly, there is a sexually dimorphic response to temperature in D. melanogaster: temperature affects only cell size in female flies while both cell size and number respond in males. Dung flies show the reverse pattern corresponding with their reversed size dimorphism. This pattern is unknown for other groups. Does sexual size dimorphism in general reflect distinct underlying growth processes? The functional consequences of different growth mechanisms have not often been considered. In fact, Zwaan et al. (2000) suggest that cellular differences between Australian and S. American clines in D. melanogaster are non-functional, the target of selection being size itself and the flies evolving via whatever genetic variation happened to be present in the ancestral population. This may be true as a fly wing (or leaf epidermis) made up of many small cells may be functionally identical to one made up of fewer large cells. However, such structural differences could have functional effects: for example on wing (or leaf) stiffness. Slade (1970), for example, found that grass grown in the shade had larger leaves (via increased cell size) that were weaker than sungrown leaves and incapable of ‘‘normal’’ erect growth. This may be due to shade leaves being thinner overall, but it is

251 also possible that fewer, larger cells are less stiff than many small cells in the same area. Whether a similar effect would happen to fly wings, and whether this would alter flight efficiency, has not been explored. Variation in muscle composition is likely to have a direct effect on performance. Arendt & Hoang (2005) found that spadefoot tadpoles reared at warm temperatures were slower swimmers, and this was correlated with their having more and larger muscle fibres due to a shift in the onset of fibre recruitment. Similarly, Clyde herring reared at warmer temperatures have slower fast-starts and show greater yaw during cruise swimming than those reared at cooler temperatures (Johnston, Temple & Vieira, 2001). Warmreared herring also have more and larger muscle fibres (Johnston et al., 1998). In addition, Rivero et al. (1993) showed that horses with superior running endurance had larger fibres of a more uniform size in the gluteus medius. Growth by itself may also be the target of selection. Atchley & Zhu (1997) argue that selection for rapid early growth in mice generally alters cell proliferation patterns while selection at later ages will primarily alter cell size (see also Atchley, Wei & Crenshaw, 2000). Thus the age-specific timing of selection on growth rate or body size may act through alternative mechanisms. It is also possible that selection acts not on a character of the whole organism (size or growth rate), but on the cells themselves. Matschak et al. (1995) provide evidence that oxygen availability, rather than temperature, is the driving force behind muscle cell size variation in Atlantic salmon embryos. Growth at higher temperatures increases metabolic rate and oxygen demand, but oxygen tension decreases with temperature in water. If smaller cells have an advantage at low oxygen levels, then this may explain why hatchling salmon have smaller cells at warmer temperatures. One major caveat must be considered in interpreting these patterns. Contribution of cell size and number to body size have typically been investigated using a single cell type within a given species. There is some indication that these patterns may not hold for all cell types or in all organs. For example, Azevedo French & Partridge (2002) looked at cell size and number in the wing, leg and cornea of the eye of D. melanogaster. They found that the plastic response to temperature in all three tissues was due to cell size (as is general for wing cells), but that when comparing populations the wings differed in cell number while the leg and eye differed in cell size. For fish, Table 2 only lists results for white (anaerobic) muscle fibres. In herring, red (aerobic) fibres do not necessarily follow the same pattern, although the specific response is inconsistent among studies (Johnston, 1993; Johnston et al., 1995, 1998). Similarly, Table 4 gives results from leaf epidermal cells; palisade cells may show very different patterns. For example, sun-exposed leaves are invariably thicker than shade leaves whether or not they have greater surface area. Increased leaf thickness may be due to increased palisade cell size (e.g. Isanogle, 1944; Cormack, 1955) or both size and number (e.g. Cormack & Gorham, 1953) even when epidermal cells are smaller (Cormack & Gorham, 1953). In addition different parts of a plant may react differently to light level; high levels increase leaf size in broad bean via both increased cell size


Jeff Arendt

252 and number but decrease internode length via decreased cell size and number (Butler, 1963). Variation among tissues may reflect different constraints on different tissues (e.g. Alexander, 1995). Recognition of such variation may be advantageous as it may provide a mechanism for explaining allometric growth. For example, fruit flies from high altitudes (Norry, Bubily & Loeschke, 2001) and latitudes (Azevedo et al., 2002) have disproportionately larger wings than those from low altitudes and latitudes. Larger wing area may compensate for lower wingbeat frequency at cool temperatures (Petavy et al., 1997; Roberts et al., 2001). However, it may also be an incidental by-product of cell shape as Kuo & Larsen (1987) showed that although wings of cool-reared D. melanogaster have a larger surface area, they are thinner. Thinner wings may also be adaptive (Ellington, 1984; Okamoto, Yasuda & Azuma 1996), but this still needs to be demonstrated. It should be noted that, although a change in cell shape may explain the disproportionate size of wings, it cannot explain the overall change in body mass with temperature (Azevedo et al., 2002). (3) Future directions It should be clear from the data reviewed here that being bigger is not merely a matter of changing body size. The entire composition of an organism may change as body size changes, and the precise mixture of cell size and number will vary from context to context. Furthermore, it is possible that some aspects of performance may change as a function of the relative contributions of cell size versus cell number. The total number of studies that examine how cell size and number contribute to body size remains small, but enough data are available to identify some potential patterns. Obvious areas for future research include: (1) Although there appear to be consistent patterns in the underlying mechanism driving body size responses to food and temperature manipulations, the number of organisms investigated so far remains small. Clearly we need data for a broader spectrum of plants and animals to determine how general these patterns are. (2) Qualitative differences in growth trajectories appear to be associated with different cellular mechanisms: crossing trajectories with differences in cell size, nested trajectories with differences in cell number. Unfortunately, growth trajectory data are sparse making it difficult to tell whether genetic differences in growth trajectories (among populations or in selection experiments) correlate with cellular mechanisms. Measuring growth trajectories may be a simple tool for inferring underlying growth processes and associated selection pressures. (3) Existing studies on D. melanogaster provide great detail on adult flies, but nothing on the pattern during development. Conversely, comparisons among fish provide information on their early development, but we do not know whether embryonic patterns translate into similar patterns in the adult. There is a clear need for a more complete picture of growth throughout development and not just at the beginning (fish) or end (D. melanogaster). (4) Currently there are few data on the functional consequences of building an organ from many small or a few

large cells and how this influences growth throughout ontogeny. (5) Many different mutations can influence body size, but little is known about their contribution to natural variation in body size. Such natural variation in size can be investigated at the molecular level via quantitative trait loci (QTL) studies and candidate gene approaches. In addition, the patterns identified in this review regarding the role of cell size or cell number in different conditions should make it easier to identify relevant genes. IV. CONCLUSIONS (1) Although body size influences most aspects of biology we know relatively little about how different individuals achieve a given size. Conventional wisdom, based on interspecific comparisons, has been that variation in body size is due to variation in cell number, but intraspecific comparisons show that cell size may be just as important. (2) Species show broadly similar responses to a given manipulation in body size, but different manipulations influence size via different cellular mechanisms. Plasticity in response to temperature tend to be achieved by changes in cell size and the response to resource levels via cell number, but there may be an interaction when both are manipulated. Selection experiments and population comparisons also show an influence of both cell size and number. (3) Past work on plasticity, selection, and population comparisons often assumed similar ecological factors to be influencing body size. Given the differences in cellular composition correlated with body size identified herein, it seems likely that either different developmental/physiological responses are important under different situations, or that the trait undergoing selection has been misidentified. Paying attention to cellular composition may thus help us to understand the evolutionary ecology of body size. (4) The shape of growth trajectories appear to be determined by the underlying growth process. At least for D. melanogaster, crossing trajectories are most common when final size depends upon cell size while nested trajectories are most common when size depends more on cell number. These patterns need to be confirmed with future studies on the shapes of growth trajectories under diverse conditions and in a wider range of organisms. V. ACKNOWLEDGEMENTS This review was greatly improved by discussion with David Reznick and his laboratory. This work was supported by NSF grant IBN-0117536. VI. REFERENCES ALAMI-DURANTE, H., BERGOT, P., ROUEL, M. & GOLDSPINK, G. (2000). Effects of environmental temperature on the development of the myotomal white muscle in larval carp (Cyprinus carpio L.). Journal of Experimental Biology 203, 3675–3688.


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