Dynamic body size evolution during speciation of predatory cichlid fishes in the Lake Malawi superradiation.

Summary1. The cichlid fish Metriaclima zebra, common in Lake Malawi, feeds by filtering plankton from the water and by brushing items from sediment covered substrata. It inhabits isolated rocky reefs among which community structure, resource availability and gene pools are likely to differ. We speculated that body size and trophic morphology of M. zebra might vary concomitantly.2. We quantified the extent of genetic, body size and trophic variation within and between populations of M. zebra from southern Lake Malawi. Specifically, we tested the hypotheses that: (i) local populations are genetically differentiated, (ii) local populations differ in jaw morphology, dentition and standard length (SL), and (iii) variation in size is correlated with variation in trophic morphology.3. Local populations of M. zebra differed in mean SL and were genetically differentiated. Moreover, populations exhibited dissimilar oral jaw morphologies and dentitions, perhaps related to differences in feeding biology. Variation in jaw shape was largely restricted to the curvature of the distal tip of the dentary. Populations were characterised by individuals with oblique, upward or downward directed gapes. Dental patterns differed in the proportion of unicuspid teeth in all rows of each jaw (dentaries and premaxillae) and the spacing of teeth in affected rows.4. Within populations, jaw and tooth shapes were correlated with body size. Smaller individuals possessed upward curving jaws and closely packed multicusped teeth, while larger individuals exhibited relatively downward‐directed jaws with increasing numbers of widely spaced unicuspid teeth.5. Metriaclima zebra populations have increased in mean SL over the last decade, in contrast to a decline among Lake Malawi pelagic cichlids. Differences in size may contribute to variation in trophic morphology and may track local environmental dynamics in this lacustrine system.

Many animal species show considerable geographic variation in average adult body sizes. Although this phenomenon offers a unique opportunity to tease apart the factors influencing body size, interpretation has proved to be difficult because several processes may contribute to the observed variation (e.g., Andrews, 1976; Case, 1978; Dunham et al., 1978). First, average body size is influenced by adult survival rates in species in which growth continues after maturity: animals may be smaller in one area than another simply because they are, on average, younger (e.g., King, 1989). Second, even if survivorships are similar among areas, so that the body-size differences are due to differences in growth patterns, there are two possible explanations for such variation in growth. Body sizes may differ either because of local genetic modifications (possibly due to adaptation) or because of a direct phenotypic effect of differing food availability on growth rates (e.g., Berry et al., 1987; Dobson and Murie, 1987; Ebenhard, 1 990). To distinguish among these alternative interpretations, we need two kinds of data on growth trajectories of animals: first from the field (to determine whether the populations differ in actual growth patterns, rather than simply survivorships) and second the response to experimental manipulation of food supply (to determine whether the observed differences in growth rates are due to genetic differences or phenotypic plasticity). This paper presents information on European grass snakes. We show that body sizes and the degree of sexual difference in body size are greatly reduced in an island population compared to the nearby mainland, that these differences are due to modified growth patterns and not just survivorship, and that the low growth rates and small asymptotic body sizes of the island snakes are a phenotypic response to local conditions (probably, low food availability). Insular populations of snakes offer some of the most dramatic examples of geographic variation in body size (e.g., Case, 1978; Schwaner, 1985; King, 1989; Shine, 1987; Schwaner and Sarre, 1988; Hasegawa and Moriguchi, 1989; Forsman, 1991). For example, Schwaner (1985) showed that body masses of adult Australian tigersnakes varied up to tenfold among adjacent islands. Correlational analyses suggest that predators attain larger sizes in areas where larger species of prey are available, and this may be true both for snakes (Schwaner, 1985; Hasegawa and Moriguchi, 1989) and for mammalian predators (Gittleman, 1985; Erlinge, 1987). Experimental studies on mammals have shown that geographic variation in body sizes may be due both to phenotypic plasticity (e.g., Dobson and Murie, 1987) and to local adaptation (e.g., Berry et al., 1987; Ebenhard, 1990). The only experimental study to address the determinants of such differences in snakes has been that of Barnett and Schwaner (1984), who raised juvenile tigersnakes. These authors documented rapid growth in captive snakes from a giant population, but obtained no comparable information on snakes from dwarf populations. We studied two populations of a nonvenomous natricine colubrid species, the grass snake (Natrix natrix), which is abundant over much of Europe (Arnold and Burton, 1978). The mainland study area was near Maryd, 15 km south of Lund in southern Sweden (55?40'N, 13?30'E). The area contains a mixture of arable land, grazed meadow, and mixed deciduous forest. Detailed data have already been published on body sizes, sexual size dimorphism, growth rates, diets and reproductive biology of grass snakes from this area (Madsen, 1983, 1987). Those papers also describe the methods used to capture, mark and measure snakes, and to obtain prey items by forced regurgitation. The same methods were used for the study of island snakes. Our island population was on Hallands Vadero (56?27'N, 12?44'E), a small (2.6 kM2) island approximately 3 km from the Swedish coast. One quarter of the island is forested, with the remainder consisting of meadows bordered by blackthorn, stony areas with juniper, and bare rock (Madsen and Stille, 1988). The two study areas are approximately 100 km apart. Geological evidence suggests that the two areas probably have been separated for several thousand years, since glaciation-induced reductions in sea level (Devoy, 1987). However, it is possible that the effective period of separation may have been longer than this (e.g., these oviparous snakes may not have existed in this region during glacial periods) or considerably briefer (due to fortuitous dispersal of snakes from one area to another). Male snakes from the island were similar to the mainland animals in mean SVL (Fig. 1; N = 22, 41; means = 52.2 versus 53.0 cm, t = 0.40, df= 61, P = 0.69) but females were much smaller on the island (N = 28, 44; means 59.7 versus 69.9 cm, t = 4.14, df= 70, P < 0.001). Indeed, some male snakes from the mainland actually attained larger sizes than did any of the females from the island population, although the mean values were lower (Fig. 1). Two-factor analysis

Selection favors larger body size in many taxa. In some species, larger individuals are more active and bolder than smaller conspecifics, but the nature of this relationship is unclear: Is body size a predictor or a consequence of behavior? Any effect of behavior on body size may be through its effect on competitive ability, suggesting that the presence of potential competitors could exaggerate or suppress this relationship. In this study, we tested whether an individual's activity rates early in life predict its future body size by measuring same-aged, sibling eastern fence lizards before (8 d) and after (8 wk) they significantly diverged in body size. We tested for an effect of conspecific presence (potential competition) on the relationship between early behavior and future body size by housing some lizards in sibling groups and others individually, using a split-clutch design. Our results reveal that individuals' activity rates do not significantly differ between 8 d and 8 wk of age. At 8 wk (but not 8 d) of age, more active siblings were also larger in both housing treatments; however, early activity rates did not predict body size later in development for either of these groups. Conversely, body size at hatching did predict size at 8 wk. Although variation in activity rates exists prior to divergence in body size, and activity and body size are correlated later in development, our results suggest that higher activity rates are unlikely to be driving body size divergence in this species. Instead, very small differences in body size at hatching appear to be compounded over time and drive much more exaggerated differences in later body size.

Intra-specific body size variation is common and often is assumed to be adaptive. Studies of body size variation among sites should include or consider environmental and ecological variables in their designs. Additionally, reciprocal transplant or common garden studies will support which variables are really contributing to the observed body size variation. This study analyzed the microgeographic body size variation in Anolis mariarum, a small lizard endemic to Antioquia, Colombia. Parameters such as body size, shape, and lepidosis variation were quantified in 217 adult A. mariarum, belonging to six populations separated by less than 80km. Results showed that significant body size variation was not related to differences among sites in mean annual temperature, but covaried with mean annual precipitation, with the largest individuals occurring in dryer sites. Mark-recapture data obtained from 115 individuals from both the wettest and dryest sites from October 2004 to April 2005 showed that growth rates were higher at the latter. Eight males from each site were captured at the end of the mark-recapture study and reared for two months under identical conditions in a common garden study. Individuals from both sites grew faster when reared in the laboratory with food provided ad libitum. Although growth rates of males from the two populations did not differ significantly in the laboratory, males from the dryest site still maintained a significantly larger asymptotic body size in their growth trajectories. Multivariate analyses also demonstrated that both males and females from the six populations differed in terms of body shape and lepidosis. However, only female body size was found to covary significantly with an environmental gradient (precipitation). A. mariarum does not conform to Bergmann's rule, but the relationship found between mean body size and asympotic growth with mean annual precipitation at these sites needs further analysis. Generally, studies of intra-specific body size variation should consider a number of additional phenotypic traits to provide stronger baseline information on the degree of overall divergence among populations, including those likely to be selectively neutral, before interpreting results of analyses on the body size differences.

The evolution of body size within and among species is predicted to be influenced by multifarious environmental factors. However, the specific drivers of body size variation have remained difficult to understand because of the wide range of proximate factors that covary with ectotherm body sizes across populations with varying local environmental conditions. Here, we used female Eremias argus lizards collected from different populations across their wide range in China, and constructed linear mixed models to assess how climatic conditions and/or available resources at different altitudes shape the geographical patterns of lizard body size across altitude. Lizard populations showed significant differences in body size across altitudes. Furthermore, we found that climatic and seasonal changes along the altitudinal gradient also explained variations in body size among populations. Specifically, body size decreased with colder and drier environmental conditions at high altitudes, reversing Bergmann's rule. Limited resources at high altitudes, measured by the low vegetative index, may also constrain body size. Therefore, our study demonstrates that multifarious environmental factors could strongly influence the intraspecific variation in organisms' body size.

The relationship between environmental gradients and patterns of geographic variation in body size has been a controversial topic for ectothermic organisms globally. To examine whether the patterns that generally hold in more temperate species also hold for tropical ones, we examined the intraspecific body size variation in three species of Neotropical frogs, Dendropsophus minutus, Hypsiboas faber and Physalaemus cuvieri, along different environmental gradients (e.g. temperature, precipitation and topography). We analysed four competing hypotheses: (i) the water availability hypothesis that predicts a negative relationship between body size and precipitation; (ii) the heat balance hypothesis that predicts a negative relationship between body size and temperature; (iii) the topography hypothesis that predicts a negative relationship between body size and altitude; and (iv) the mixed-effect hypothesis that predicts that individuals occurring in wet and cold sites would be larger than individuals occurring in dry and warm sites. The spatial pattern of geographic variation in body size among populations of H. faber was associated with the mixed-effect hypothesis. In localities with low precipitation seasonality and cold conditions, H. faber individuals were larger than in localities with high precipitation seasonality and warm conditions. Variation in the body size of D. minutus was the opposite of that predicted by the heat balance hypothesis. Individuals in localities with high temperatures were larger than in localities with low temperatures. On the other hand, variation in the body size of P. cuvieri was not associated with the variables used in this study. Our results suggest that intraspecific variation in anuran body size is more dependent on species-specific response than on the region (i.e. temperate or tropical) where they occur.

SUMMARY Lake Malawi (LM) cichlids have undergone heterochronic shifts in the expression of their cone opsin genes, the genes responsible for color vision. These shifts have generated species with short-, middle-, and long-wavelength-sensitive cone photoreceptors and visual systems. However, it is unclear when during the evolution of African cichlids these shifts occurred, or whether they could account for similar short- and middle-wavelength-sensitive profiles among unrelated cichlids in Lake Tanganyika (LT). To address these questions, we surveyed opsin expression in developing fry of two African cichlids, Astatotilapia burtoni from LT and Melanochromis auratus from LM. We found that A. burtoni expresses a series of three different single-cone opsins over the course of development, while M. auratus exhibits variation in the expression of only two. Neither A. burtoni nor M. auratus exhibits much variation in the expression of its double-cone opsins. These patterns reveal that A. burtoni exhibits progressive development in the sensitivity of its single-cone photoreceptors, but direct development in the sensitivity of its double-cone photoreceptors. M. auratus exhibits neotenic development in the sensitivity of both photoreceptor sets. Given the intermediate phylogenetic placement of A. burtoni between cichlids from LT and LM, our results suggest that the ancestor of LM's cichlids exhibited a progressive developmental pattern of opsin expression. These results indicate that the heterochronic shifts which produced the short- and middle-wavelength-sensitive profiles of LM's cichlids occurred recently, and suggest that the presence of similar profiles among LT's cichlids are due to parallel heterochronic shifts.

Body size is an integrative trait with substantial fitness consequences in animals. Geographical clines in body size have fascinated biologists because of their potential to provide insight into the mechanisms governing local adaptation and phenotypic plasticity. In this complex study, we focused on variation in body size of Silpha carinata (Coleoptera: Silphidae) along elevation gradients in Central Europe. Altitudinal clines were investigated separately for males and females as sex‐specific responses to environmental conditions are documented for a variety of insect species. To identify potential underlying mechanisms responsible for observed patterns, a common garden experiment and investigation of within‐population variation in body size were performed. Body size of S. carinata recorded in nature sharply decreased with increasing altitude in both genders, whereas sexual size dimorphism did not change with altitude. The degree of within‐population variation in body size recorded in nature did not change with altitude. Under standardized laboratory conditions, higher altitude females produced smaller eggs than those from lower altitude. This size difference persisted to the very end of the larval period. Unfortunately, only few offspring survived till adulthood in the laboratory and thus precise analysis of offspring adult sizes was unfeasible, but between‐population differences in body size seems to persist to adulthood. The observed converse Bergmann's cline in S. carinata fits well with what has been predicted for large, carnivorous, univoltine insect species. Until now, investigation of within‐population variation in body size is rare in insects, and future complementary studies focused on this issue are highly needed as within‐population variation could explain body size patterns observed at between‐population level.

Comment on “Abrupt change in tropical African climate linked to the bipolar seesaw over the past 55,000 years” by E. T. Brown, T. C. Johnson, C. A. Scholz, A. S. Cohen, and J. W. King

Although variation in body size has been recently reported in stingless bees (Meliponini), empirical evidence evaluating possible factors related to such variation is lacking, and thus it is not clear if it may have an adaptive significance. We evaluated if variation in the body size and weight of workers of stingless bees fluctuates across a seasonal pattern and if this could be related to characteristics of the food consumed during the larval stage. The weight of larval provisions, their protein, and sugar content were evaluated in four colonies of Nannotrigona perilampoides every 2 months across 1 year. Worker-destined larvae from the same combs were allowed to develop and were sampled as callow workers to determine their weight and size using morphometric data. The weight and size of workers were highly correlated and varied across the seasons in established colonies, suggesting that size variation cycles across the year in stingless bees. An increase in the protein content and, to a lesser degree, the quantity of larval food were positively linked to variation in body weight and size; food with richer protein content resulted in larger and heavier workers. This study provides the first evidence of an effect of the quantity and composition of larval food on the size of workers in stingless bees. Although body weight and size of workers differed across seasons, they were not readily noticeable as changes seem to occur as a continuum across the year. Since size polymorphism was of a larger magnitude across time but not within age cohorts and as it was highly determined by food resources, it may not be an adaptive feature in stingless bees. However, more studies are needed to determine the role of the cyclical change in worker body size on colony performance and thus its adaptive significance in stingless bees.

Snakes are ecologically and morphologically plastic organisms that exhibit extensive variations in body size and body condition in response to environmental factors. Documenting inter-population variations is important to describe species comprehensively across their distribution range and to monitor trends over time (e.g. decreasing body condition due to alteration of habitat). Thus, we analyzed the influence of population and sex on body size and body condition in three populations of nose-horned vipers (Vipera ammodytes) in Serbia. In one population, males were larger than females (F1, 39=4.802, p=0.034), but not in the two other populations (F1, 36=0.075, p=0.786; F1, 21=0.018, p=0.893). Females exhibited higher body condition (residual values from the regression of log-body mass against log-body size) than males (F1, 90=10.444, p=0.002); this sex difference was not found in one population when analyzed separately (F1, 35=1.834, p=0.184). Moreover, we found strong inter-population differences in mean body size and mean body condition (F2, 96=8.822, p&amp;lt;0.001 and F2, 90=10.319, p=0.001, respectively). While inter-population difference in body size was driven by males, inter-population difference in body condition was driven by females. These results suggest that, in this species, body size might be an important determinant of mating success in males, while body condition may play a major role in female fecundity.

Cichlid fishes have evolved tremendous morphological and behavioral diversity in the waters of East Africa. Within each of the Great Lakes Tanganyika, Malawi, and Victoria, the phenomena of hybridization and retention of ancestral polymorphism explain allele sharing across species. Here, we explore the sharing of single nucleotide polymorphisms (SNPs) between the major East African cichlid assemblages. A set of approximately 200 genic and nongenic SNPs was ascertained in five Lake Malawi species and genotyped in a diverse collection of ∼160 species from across Africa. We observed segregating polymorphism outside of the Malawi lineage for more than 50% of these loci; this holds similarly for genic versus nongenic SNPs, as well as for SNPs at putative CpG versus non-CpG sites. Bayesian and principal component analyses of genetic structure in the data demonstrate that the Lake Malawi endemic flock is not monophyletic and that river species have likely contributed significantly to Malawi genomes. Coalescent simulations support the hypothesis that river cichlids have transported polymorphism between lake assemblages. We observed strong genetic differentiation between Malawi lineages for approximately 8% of loci, with contributions from both genic and nongenic SNPs. Notably, more than half of these outlier loci between Malawi groups are polymorphic outside of the lake. Cichlid fishes have evolved diversity in Lake Malawi as new mutations combined with standing genetic variation shared across East Africa.

Geological, climate, and ecosystem changes in Africa probably influenced speciation of Afrotropical freshwater crabs. In total, the subfamily Potamonautinae comprises over 120 species, and this diversity provides a valuable opportunity to explore speciation processes. Here we study diversification of potamonautid crabs in the Lake Malawi catchment, and investigate whether speciation has taken place across a lake–river boundary. Specifically, we reconstruct evolutionary relationships of the Malawi blue crab, Arcopotamonautes orbitospinus (Cunnington, 1907), an endemic of Lake Malawi, and of A. montivagus (Chace, 1953) from rivers and streams draining into Lake Malawi, and smaller lakes within this catchment. Our phylogenetic analysis of over 28 000 single nucleotide polymorphisms shows a monophyletic A. orbitospinus nested within a clade otherwise comprising A. montivagus from across the Lake Malawi catchment (A. montivagus Group I). We also identified a second allopatric clade of A. montivagus from the Rungwe mountains of Tanzania, and neighbouring Zambia (A. montivagus Group II). Morphological differences were apparent between all three groups. Collectively these results show A. montivagus is a paraphyletic riverine taxon that has diversified in allopatry, and that this species entered Lake Malawi and seeded the specialized heavily armoured lacustrine species, A. orbitospinus. We hypothesize that formation of deep-water conditions within Lake Malawi, together with differences in predation pressures between the rivers and lake, provided ecological opportunities for natural selection to drive speciation across the lake–river boundary. We conclude that geographical separation and ecological adaptation are potentially important drivers of evolutionary diversification in these enigmatic freshwater crabs.

ABSTRACTAim To determine how well variation in median body size of avian assemblages is predicted by (1) the environmental models usually employed in analyses of Bergmann's rule and (2) random sampling from the regional body size frequency distribution. If body size frequency distributions of local assemblages represent a random sample of a regional frequency distribution, then geographical variation in body sizes of assemblages might be a consequence of the determinants of spatial variation in species richness rather than direct influences on body size per se.Location Southern Africa.Methods Median body masses (as a measure of body size) of avian assemblages were calculated for quarter‐degree grid cells across South Africa and Lesotho. The relationship between median body mass and four environmental variables (minimum and maximum monthly temperatures, precipitation and seasonality in the normalized difference vegetation index, as a measure of seasonality in productivity) was examined using general linear models first without taking spatial autocorrelation into account, and then accounting for it by fitting an exponential spatial covariance structure. Model fit was assessed using the Akaike information criterion and Akaike weights. At each species richness value, random assemblages were sampled by either drawing species randomly from the regional body mass frequency distribution, or drawing species from the regional body mass frequency distribution with a probability proportional to their geographical distribution in the area. The ability of randomizations to predict actual body masses was examined using two‐tailed Fisher exact tests.Results Seasonality in productivity was the only environmental variable that remained a significant predictor of body mass variation in spatially explicit models, though the positive relationship was weak. When species richness was included in the models it remained the only significant predictor of size variation. Randomizations predicted median body mass poorly at low species richness, but well at high richness.Main conclusions Environmental models that have previously been proposed explain little of the variation in body mass across avian assemblages in South Africa. However, much of the variation in the median mass of assemblages could be predicted by randomly drawing species from the regional body mass frequency distribution, particularly using randomizations in which all species were drawn from the regional body mass frequency distribution with equal probability and at high species richness values. This outcome emphasizes the need to consider null expectations in investigations of the geographical variation in body size together with the probable environmental mechanisms underlying spatial variation in average size. Moreover, it suggests that in the South African avifauna, spatial variation in the body sizes of assemblages may be determined indirectly by the factors that influence geographical variation in species richness.

1. The egg size of insects can vary depending on maternal body size or resource status, and it may influence offspring body size by determining initial resource level.2. The giant rhinoceros beetle Trypoxylus dichotomus exhibits considerable variation in body size, some of which is attributed to the variation in larval food (humus) quality, although a substantial amount of variation in body size remains unexplained. In the present study, changes in the egg size and offspring body size in response to several maternal variables were examined (i.e. body size, age, and, nutritional status).3. Nutritional intake of the females during the adult stage did not affect the egg size. Larvae hatched from small eggs partially recovered from the initial disadvantage during their ontogenetic processes by increasing growth rate (i.e. compensatory growth); however, there was still a positive relationship between egg size and pupal body size.4. Older females produced small eggs, but because of compensatory growth, the pupae were no longer small. By contrast, due to a lack of compensatory growth, small females produced small eggs as well as small pupae.5. These results suggest that maternal body size affects offspring body size through effects on egg size. This transgenerational effect may account for some of the variation in adult body size of T. dichotomus.