Evolution of body size in Galapagos marine iguanas

Abstract

Body size is one of the most important traits of organisms and allows predictions of an individual's morphology, physiology, behaviour and life history. However, explaining the evolution of complex traits such as body size is difficult because a plethora of other traits influence body size. Here I review what we know about the evolution of body size in a group of island reptiles and try to generalize about the mechanisms that shape body size. Galapagos marine iguanas occupy all 13 larger islands in this Pacific archipelago and have maximum island body weights between 900 and 12 000g. The distribution of body sizes does not match mitochondrial clades, indicating that body size evolves independently of genetic relatedness. Marine iguanas lack intra- and inter-specific food competition and predators are not size-specific, discounting these factors as selective agents influencing body size. Instead I hypothesize that body size reflects the trade-offs between sexual and natural selection. We found that sexual selection continuously favours larger body sizes. Large males establish display territories and some gain over-proportional reproductive success in the iguanas' mating aggregations. Females select males based on size and activity and are thus responsible for the observed mating skew. However, large individuals are strongly selected against during El Niño-related famines when dietary algae disappear from the intertidal foraging areas. We showed that differences in algae sward ('pasture') heights and thermal constraints on large size are causally responsible for differences in maximum body size among populations. I hypothesize that body size in many animal species reflects a trade-off between foraging constraints and sexual selection and suggest that future research could focus on physiological and genetic mechanisms determining body size in wild animals. Furthermore, evolutionary stable body size distributions within populations should be analysed to better understand selection pressures on individual body size.

Figure 1

The island area in Galapagos appears to predict the maximum snout-to-vent length (SVL) of marine iguanas. Only populations are shown for which measurements existed in 1906 (filled circles) and 1997 (open squares). The lines represent best fit quadratic regressions.

Figure 2

The algae sward height as measured in the intertidal zone where adult marine iguanas forage predicts maximum snout-to-vent length (SVL) of marine iguanas. Note that in this graph, small islands (Genovesa) also have small body sizes and large islands (Fernandina) have large body sizes (compare with figure 1). Filled circles show non-El Niño data (1998) and open squares show El Niño data (1999). The line represents a linear regression.

Figure 3

(a) The maximum ever measured body condition for each mm body size for marine iguanas on two islands, Genovesa and Santa Fe. Circles show data for Santa Fe, squares data for Genovesa—open symbols are males and closed symbols, females. The lines represent regression lines that start at the deflection point when maximum body conditions start to decline (above a threshold body size). (b) The intake per bite, corrected for the metabolic body mass generally decreases towards larger body size, but no decrease can be detected within the largest males of each island. To calculate mass-specfic intake we assume an allometric scaling of energy expenditure of 0.8. Redrawn from Wikelski & Trillmich (1997).

Figure 4

Annual survival estimates as determined from mark–recapture data on Genovesa and Santa Fe islands from February 1991 to March 1992. Survival data are estimates from Jolly–Seber survival models. Circles show data for Santa Fe, squares data for Genovesa, filled symbols are males, open symbols females. Redrawn from Wikelski & Trillmich (1997).

Figure 5

Food intake (dashed and solid lines) of marine iguanas from two islands (Genovesa, Santa Fe) differs dramatically, both between islands and between seasons. Iguanas on Santa Fe have much higher food intakes than Genovesa iguanas. Food intake is lower during El Niño periods (solid line; 1991/92) compared to a ‘normal’ year (dashed line, 1992/93). The regression lines from food intake cross the regression line from energy expenditure (field metabolic rate, FMR) at much lower body sizes in Genovesa compared to Santa Fe. The predicted maximum body mass is much lower on Genovesa than on Santa Fe, and lower during El Niños than during normal years. Regressions lines only are shown here for graphical clarity. Redrawn from Wikelski et al. (1997).

Figure 6

Mean standard operative temperature and mean algae pasture height predict the maximum body mass of marine iguanas in the Galapagos archipelago. Isocline lines indicate maximum body mass in grams. The grey ovals indicate the range of average values predicted from the measurement of environmental parameters in the field, while the vertical bars show the range of maximum body masses found in the wild. The black area to the left top of the graph identifies the range of environmental conditions when the digestive system of the iguanas cannot cope any more with maximum amount of ingested food, such as when the environmental temperature falls too much or when the algae pasture height increases too much. Redrawn from Wikelski & Carbone (2004).

Figure 7

On both Santa Fe and Genovesa island, males of large body size relative to the rest of the population achieve high numbers of copulation. Filled circles show data for Santa Fe and open squares show data for Genovesa.

Figure 8

(a) Clutch mass (top panel) and clutch size (inset) increase with female mass. All females below 400 g body mass are from Genovesa island, the remainder from Santa Fe. (b) The survival of young marine iguanas depends on their initial size at hatching (Santa Fe iguanas only). Each data point represents the average survival per mm SVL for a cohort of 1285 marine iguanas hatched in 1988. Redrawn from Wikelski & Romero (2003).