The evolution of island gigantism and body size variation in tortoises and turtles

Extant chelonians (turtles and tortoises) span almost four orders of magnitude of body size, including the startling examples of gigantism seen in the tortoises of the Galapagos and Seychelles islands. However, the evolutionary determinants of size diversity in chelonians are poorly understood. We present a comparative analysis of body size evolution in turtles and tortoises within a phylogenetic framework. Our results reveal a pronounced relationship between habitat and optimal body size in chelonians. We found strong evidence for separate, larger optimal body sizes for sea turtles and island tortoises, the latter showing support for the rule of island gigantism in non-mammalian amniotes. Optimal sizes for freshwater and mainland terrestrial turtles are similar and smaller, although the range of body size variation in these forms is qualitatively greater. The greater number of potential niches in freshwater and terrestrial environments may mean that body size relationships are more complicated in these habitats.     

The tempo of genetic evolution in birds: body mass and climate effects

Aim Negative relationships between body mass and substitution rates have previously been reported. However, most of these studies have involved contrasted taxa that, due to their highly divergent phylogenetic histories, also differ in many additional characteristics other than mass. In particular, there has been little examination of the potentially confounding effects of climate or population size. Here we test for differences in rates of microevolution among bird species that, although differing in mass, are nonetheless very closely related phylogenetic pairs. We additionally tested for latitudinal/elevational and population size effects across these contrasts. Location Global. Methods The tempo of microevolution within the cytochrome b gene of mitochondrial DNA was compared between closely related bird species that differed in body mass, using 130 phylogenetically independent species pairs. In order to minimize climate effects, pairs not having overlapping latitudinal ranges were discarded. In addition, a subset of pairs was identified and analysed that involved comparisons between species that have different latitudinal or elevational midpoints. Results Species with smaller mass had substitution rates marginally faster than those with larger mass (small : large median ratio = 1.05). However, this result was only statistically significant when data were pruned to eliminate comparisons in which population or range size also varied substantially between contrasted species. Latitude and elevation had a much stronger association with substitution rates than body mass within the subset of pairs (n = 30) that also differed in their spatial distributions: lower elevation or latitude species had substantially more substitutions than those at higher latitudes or elevations (low : high ratio = 1.35). Furthermore, when the dataset was pruned of pairs in which body mass was confounded by latitude or elevation, the body mass effect was eliminated. Main conclusions Body mass is known to correlate with latitude, so that the latitudinal/elevational association with microevolution we found might either be additive to, or causal of, the body mass effect. These results are consistent with the evolutionary speed hypothesis, which suggests that latitudinal diversity gradients derive from variation in the rate of microevolution. Our findings also serve to raise concerns about biogeographical studies that use genetic distances between taxa to estimate time since divergence.     

Of mice and mammoths: evaluations of causal explanations for body size evolution in insular mammals

Aim We investigated the hypothesis that the insular body size of mammals results from selective forces whose influence varies with characteristics of the focal islands and the focal species, and with interactions among species (ecological displacement and release). Location Islands world‐wide. Methods We assembled data on the geographic characteristics (area, isolation, maximum elevation, latitude) and climate (annual averages and seasonality of temperature and precipitation) of islands, and on the ecological and morphological characteristics of focal species (number of mammalian competitors and predators, diet, body size of mainland reference populations) that were most relevant to our hypothesis (385 insular populations from 98 species of extant, non‐volant mammals across 248 islands). We used regression tree analyses to examine the hypothesized contextual importance of these factors in explaining variation in the insular body size of mammals. Results The results of regression tree analyses were consistent with predictions based on hypotheses of ecological release (more pronounced changes in body size on islands lacking mammalian competitors or predators), immigrant selection (more pronounced gigantism in small species inhabiting more isolated islands), thermoregulation and endurance during periods of climatic or environmental stress (more pronounced gigantism of small mammals on islands of higher latitudes or on those with colder and more seasonal climates), and resource subsidies (larger body size for mammals that utilize aquatic prey). The results, however, were not consistent with a prediction based on resource limitation and island area; that is, the insular body size of large mammals was not positively correlated with island area. Main conclusions These results support the hypothesis that the body size evolution of insular mammals is influenced by a combination of selective forces whose relative importance and nature of influence are contextual. While there may exist a theoretical optimal body size for mammals in general, the optimum for a particular insular population varies in a predictable manner with characteristics of the islands and the species, and with interactions among species. This study did, however, produce some unanticipated results that merit further study – patterns associated with Bergmann’s rule are amplified on islands, and the body size of small mammals appears to peak at intermediate and not maximum values of latitude and island isolation.     

Evolution and ecology of lizard body sizes

Aim Body size is instrumental in influencing animal physiology, morphology, ecology and evolution, as well as extinction risk. I examine several hypotheses regarding the influence of body size on lizard evolution and extinction risk, assessing whether body size influences, or is influenced by, species richness, herbivory, island dwelling and extinction risk. Location World‐wide. Methods I used literature data and measurements of museum and live specimens to estimate lizard body size distributions. Results I obtained body size data for 99% of the world's lizard species. The body size–frequency distribution is highly modal and right skewed and similar distributions characterize most lizard families and lizard assemblages across biogeographical realms. There is a strong negative correlation between mean body size within families and species richness. Herbivorous lizards are larger than omnivorous and carnivorous ones, and aquatic lizards are larger than non‐aquatic species. Diurnal activity is associated with small body size. Insular lizards tend towards both extremes of the size spectrum. Extinction risk increases with body size of species for which risk has been assessed. Main conclusions Small size seems to promote fast diversification of disparate body plans. The absence of mammalian predators allows insular lizards to attain larger body sizes by means of release from predation and allows them to evolve into the top predator niche. Island living also promotes a high frequency of herbivory, which is also associated with large size. Aquatic and nocturnal lizards probably evolve large size because of thermal constraints. The association between large size and high extinction risk, however, probably reflects a bias in the species in which risk has been studied.     

Of mice and mammoths: generality and antiquity of the island rule

Aim

We assessed the generality of the island rule in a database comprising 1593 populations of insular mammals (439 species, including 63 species of fossil mammals), and tested whether observed patterns differed among taxonomic and functional groups.

Location

Islands world‐wide.

Methods

We measured museum specimens (fossil mammals) and reviewed the literature to compile a database of insular animal body size (S_i = mean mass of individuals from an insular population divided by that of individuals from an ancestral or mainland population, M). We used linear regressions to investigate the relationship between S_i and M, and ANCOVA to compare trends among taxonomic and functional groups.

Results

S_i was significantly and negatively related to the mass of the ancestral or mainland population across all mammals and within all orders of extant mammals analysed, and across palaeo‐insular (considered separately) mammals as well. Insular body size was significantly smaller for bats and insectivores than for the other orders studied here, but significantly larger for mammals that utilized aquatic prey than for those restricted to terrestrial prey.

Main conclusions

The island rule appears to be a pervasive pattern, exhibited by mammals from a broad range of orders, functional groups and time periods. There remains, however, much scatter about the general trend; this residual variation may be highly informative as it appears consistent with differences among species, islands and environmental characteristics hypothesized to influence body size evolution in general. The more pronounced gigantism and dwarfism of palaeo‐insular mammals, in particular, is consistent with a hypothesis that emphasizes the importance of ecological interactions (time in isolation from mammalian predators and competitors was 0.1 to > 1.0 Myr for palaeo‐insular mammals, but < 0.01 Myr for extant populations of insular mammals). While ecological displacement may be a major force driving diversification in body size in high‐diversity biotas, ecological release in species‐poor biotas often results in the convergence of insular mammals on the size of intermediate but absent species.     

Cope's rule and the adaptive landscape of dinosaur body size evolution

The largest known dinosaurs weighed at least 20 million times as much as the smallest, indicating exceptional phenotypic divergence. Previous studies have focused on extreme giant sizes, tests of Cope's rule, and miniaturization on the line leading to birds. We use non‐uniform macroevolutionary models based on Ornstein–Uhlenbeck and trend processes to unify these observations, asking: what patterns of evolutionary rates, directionality and constraint explain the diversification of dinosaur body mass? We find that dinosaur evolution is constrained by attraction to discrete body size optima that undergo rare, but abrupt, evolutionary shifts. This model explains both the rarity of multi‐lineage directional trends, and the occurrence of abrupt directional excursions during the origins of groups such as tiny pygostylian birds and giant sauropods. Most expansion of trait space results from rare, constraint‐breaking innovations in just a small number of lineages. These lineages shifted rapidly into novel regions of trait space, occasionally to small sizes, but most often to large or giant sizes. As with Cenozoic mammals, intermediate body sizes were typically attained only transiently by lineages on a trajectory from small to large size. This demonstrates that bimodality in the macroevolutionary adaptive landscape for land vertebrates has existed for more than 200 million years.     

What are mycoplasmas: The relationship of tempo and mode in bacterial evolution

Summary In phenotype the mycoplasmas are very different from ordinary bacteria. However, genotypically (i.e., phylogenetically) they are not. On the basis of ribosomal RNA homologies the mycoplasmas belong with the clostridia, and indeed havespecific clostridial relatives. Mycoplasmas are, however, unlike almost all other bacteria in the evolutionary characteristics of their ribosomal RNAs. These RNAs contain relatively few of the highly conserved oligonucleotide sequences characteristic of normal eubacterial ribosomal RNAs. This is interpreted to be a reflection of an elevated mutation rate in mycoplasma lines of descent. A general consequence of this would be that the variation associated with a mycoplasma population is augmented both in number and kind, which in turn would lead to an unusual evolutionary course, one unique in all respects. Mycoplasmas, then, are actually tachytelic bacteria. The unusual evolutionary characteristics of their ribosomal RNAs are the imprints of their rapid evolution.     

The evolution of mammal body sizes: responses to Cenozoic climate change in North American mammals

Explanations for the evolution of body size in mammals have remained surprisingly elusive despite the central importance of body size in evolutionary biology. Here, we present a model which argues that the body sizes of Nearctic mammals were moulded by Cenozoic climate and vegetation changes. Following the early Eocene Climate Optimum, forests retreated and gave way to open woodland and savannah landscapes, followed later by grasslands. Many herbivores that radiated in these new landscapes underwent a switch from browsing to grazing associated with increased unguligrade cursoriality and body size, the latter driven by the energetics and constraints of cellulose digestion (fermentation). Carnivores also increased in size and digitigrade, cursorial capacity to occupy a size distribution allowing the capture of prey of the widest range of body sizes. With the emergence of larger, faster carnivores, plantigrade mammals were constrained from evolving to large body sizes and most remained smaller than 1 kg throughout the middle Cenozoic. We find no consistent support for either Cope's Rule or Bergmann's Rule in plantigrade mammals, the largest locomotor guild (n = 1186, 59% of species in the database). Some cold‐specialist plantigrade mammals, such as beavers and marmots, showed dramatic increases in body mass following the Miocene Climate Optimum which may, however, be partially explained by Bergmann's rule. This study reemphasizes the necessity of considering the evolutionary history and resultant form and function of mammalian morphotypes when attempting to understand contemporary mammalian body size distributions.     

Patterns of maximum body size evolution in Cenozoic land mammals: eco-evolutionary processes and abiotic forcing

There is accumulating evidence that macroevolutionary patterns of mammal evolution during the Cenozoic follow similar trajectories on different continents. This would suggest that such patterns are strongly determined by global abiotic factors, such as climate, or by basic eco-evolutionary processes such as filling of niches by specialization. The similarity of pattern would be expected to extend to the history of individual clades. Here, we investigate the temporal distribution of maximum size observed within individual orders globally and on separate continents. While the maximum size of individual orders of large land mammals show differences and comprise several families, the times at which orders reach their maximum size over time show strong congruence, peaking in the Middle Eocene, the Oligocene and the Plio-Pleistocene. The Eocene peak occurs when global temperature and land mammal diversity are high and is best explained as a result of niche expansion rather than abiotic forcing. Since the Eocene, there is a significant correlation between maximum size frequency and global temperature proxy. The Oligocene peak is not statistically significant and may in part be due to sampling issues. The peak in the Plio-Pleistocene occurs when global temperature and land mammal diversity are low, it is statistically the most robust one and it is best explained by global cooling. We conclude that the macroevolutionary patterns observed are a result of the interplay between eco-evolutionary processes and abiotic forcing.     

Cope's rule and the evolution of body size in Pinnipedimorpha (Mammalia: Carnivora)

Cope's rule describes the evolutionary trend for animal lineages to increase in body size over time. In this study, we tested the validity of Cope's rule for a marine mammal clade, the Pinnipedimorpha, which includes the extinct Desmatophocidae, and extant Phocidae (earless seals), Otariidae (fur seals and sea lions), and Odobenidae (walruses). We tested for the presence of Cope's rule by compiling a large dataset of body size data for extant and fossil pinnipeds and then examined how body size evolved through time. We found that there was a positive relationship between geologic age and body size. However, this trend is the result of differences between early assemblages of small-bodied pinnipeds (Oligocene to early Miocene) and later assemblages (middle Miocene to Pliocene) for which species exhibited greater size diversity. No significant differences were found between the number of increases or decreases in body size within Pinnipedimorpha or within specific pinniped clades. This suggests that the pinniped body size increase was driven by passive diversification into vacant niche space, with the common ancestor of Pinnipedimorpha occurring near the minimum adult body size possible for a marine mammal. Based upon the above results, the evolutionary history of pinnipeds does not follow Cope's rule.     

Directed evolution of a bacterial alpha-amylase: toward enhanced pH-performance and higher specific activity

alpha-Amylases, in particular, microbial alpha-amylases, are widely used in industrial processes such as starch liquefaction and pulp processes, and more recently in detergency. Due to the need for alpha-amylases with high specific activity and activity at alkaline pH, which are critical parameters, for example, for the use in detergents, we have enhanced the alpha-amylase from Bacillus amyloliquefaciens (BAA). The genes coding for the wild-type BAA and the mutants BAA S201N and BAA N297D were subjected to error-prone PCR and gene shuffling. For the screening of mutants we developed a novel, reliable assay suitable for high throughput screening based on the Phadebas assay. One mutant (BAA 42) has an optimal activity at pH 7, corresponding to a shift of one pH unit compared to the wild type. BAA 42 is active over a broader pH range than the wild type, resulting in a 5-fold higher activity at pH 10. In addition, the activity in periplasmic extracts and the specific activity increased 4- and 1.5-fold, respectively. Another mutant (BAA 29) possesses a wild-type-like pH profile but possesses a 40-fold higher activity in periplasmic extracts and a 9-fold higher specific activity. The comparison of the amino acid sequences of these two mutants with other homologous microbial alpha-amylases revealed the mutation of the highly conserved residues W194R, S197P, and A230V. In addition, three further mutations were found K406R, N414S, and E356D, the latter being present in other bacterial alpha-amylases.     

The evolution of reaction norms: simple models for age and size at maturity

This paper presents a simple model for the evolution of reaction norms for age and size at maturity that predicts reaction norms with a variety of shapes. Using realistic parameter values the model predicts reaction norms close to those observed in Drosophila. The major assumptions of the model are: 1) that net reproductive rate is maximized, 2) that growth is determinate, and 3) that mortality rates are independent of age and size at maturity. If, additionally, juvenile mortality is uncorrelated with a growth coefficient, k, the model predicts that selection favors maturation later at a smaller size when k is reduced by environmental factors and that decreased juvenile mortality leads to delayed maturity. These two predictions conform with those found by previous models using other measures of fitness. Correlations between k and juvenile mortality can change the shape of the predicted reaction norm. Depending on the precise form of the correlation, the model can predict done- or bowl-shaped reaction norms and can predict delayed or earlier maturity as k decreases. These shapes are qualitatively different from those predicted by previous models that used different fitness measures. Systematic estimates of the parameter values for this and for related models are required to determine the appropriate fitness measure for models of reaction norms.     

Sunning themselves in heaps,knots, and snarls: The extraordinary abundance and demography of island watersnakes

Snakes represent a sizable fraction of vertebrate biodiversity, but until recently, data on their demography have been sparse. Consequently, generalizations regarding patterns of variation are weak and the potential for population projections is limited. We address this information gap through an analysis of spatial and temporal variation in demography (population size, annual survival, and realized population growth) of the Lake Erie Watersnake, Nerodia sipedon insularum, and a review of snake survival more generally. Our study spans a period during which the Lake Erie Watersnake was listed as threatened under the U.S. Endangered Species Act, recovered, and was delisted. We collected capture–mark–recapture data at 14 study sites over 20 years, accruing 20,000 captures of 13,800 individually marked adults. Lake Erie Watersnakes achieve extraordinary abundance, averaging 520 adults per km of shoreline (ca. 260 adult per ha) at our study sites (range = 160–1,600 adults per km; ca. 80–800 adults per ha) and surpassing population recovery and postdelisting monitoring criteria. Annual survival averages 0.68 among adult females and 0.76 among adult males, varies among sites, and is positively correlated with body size among study sites. Temporal process variance in annual survival is low, averaging 0.0011 or less than 4% of total variance; thus, stochasticity in annual survival may be of minor significance to snake extinction risk. Estimates of realized population growth indicate that population size has been stable or increasing over the course of our study. More generally, snake annual survival overlaps broadly across continents, climate zones, families, subfamilies, reproductive modes, body size categories, maturation categories, and parity categories. Differences in survival in relation to size, parity, and maturation are in the directions predicted by life history theory but are of small magnitude with much variation around median values. Overall, annual survival appears to be quite plastic, varying with food availability, habitat quality, and other ecological variables.     

The evolution of the phenotypic covariance matrix: evidence for selection and drift in Melanoplus

Phenotypic variation in trait means is a common observation for geographically separated populations. Such variation is typically retained under common garden conditions, indicating that there has been evolutionary change in the populations, as a result of selection and/or drift. Much less frequently studied is variation in the phenotypic covariance matrix (hereafter, P matrix), although this is an important component of evolutionary change. In this paper, we examine variation in the phenotypic means and P matrices in two species of grasshopper, Melanoplus sanguinipes and M. devastator. Using the P matrices estimated for 14 populations of M. sanguinipes and three populations of M. devastator we find that (1) significant differences between the sexes can be attributed to scaling effects; (2) there is no significant difference between the two species; (3) there are highly significant differences among populations that cannot be accounted for by scaling effects; (4) these differences are a consequence of statistically significant patterns of covariation with geographic and environmental factors, phenotypic variances and covariances increasing with increased temperature but decreasing with increased latitude and altitude. This covariation suggests that selection has been important in the evolution of the P matrix in these populations Finally, we find a significant positive correlation between the average difference between matrices and the genetic distance between the populations, indicating that drift has caused some of the variation in the P matrices.     

The evolution of phenotypic plasticity in spatially structured environments: implications of intraspecific competition, plasticity costs and environmental characteristics

We model the evolution of reaction norms focusing on three aspects: frequency-dependent selection arising from resource competition, maintenance and production costs of phenotypic plasticity, and three characteristics of environmental heterogeneity (frequency of environments, their intrinsic carrying capacity and the sensitivity to phenotypic maladaptation in these environments). We show that (i) reaction norms evolve so as to trade adaptation for acquiring resources against cost avoidance; (ii) maintenance costs cause reaction norms to better adapt to frequent rather than to infrequent environments, whereas production costs do not; and (iii) evolved reaction norms confer better adaptation to environments with low rather than with high intrinsic carrying capacity. The two previous findings contradict earlier theoretical results and originate from two previously unexplored features that are included in our model. First, production costs of phenotypic plasticity are only incurred when a given phenotype is actually produced. Therefore, they are proportional to the frequency of environments, and these frequencies thus affect the selection pressure to avoid costs just as much as the selection pressure to improve adaptation. This prevents the frequency of environments from affecting the evolving reaction norm. Secondly, our model describes the evolution of plasticity for a phenotype determining an individual's capability to acquire resources, and thus its realized carrying capacity. When individuals are distributed randomly across environments, they cannot avoid experiencing environments with intrinsically low carrying capacity. As selection pressures arising from the need to improve adaptation are stronger under such extreme conditions than under mild ones, better adaptation to environments with low rather than with high intrinsic carrying capacity results.