Fluctuating selection and its (elusive) evolutionary consequences in a wild rodent population

Temporal fluctuations in the strength and direction of selection are often proposed as a mechanism that slows down evolution, both over geological and contemporary timescales. Both the prevalence of fluctuating selection and its relevance for evolutionary dynamics remain poorly understood however, especially on contemporary timescales: unbiased empirical estimates of variation in selection are scarce, and the question of how much of the variation in selection translates into variation in genetic change has largely been ignored. Using long‐term individual‐based data for a wild rodent population, we quantify the magnitude of fluctuating selection on body size. Subsequently, we estimate the evolutionary dynamics of size and test for a link between fluctuating selection and evolution. We show that, over the past 11 years, phenotypic selection on body size has fluctuated significantly. However, the strength and direction of genetic change have remained largely constant over the study period; that is, the rate of genetic change was similar in years where selection favoured heavier vs. lighter individuals. This result suggests that over shorter timescales, fluctuating selection does not necessarily translate into fluctuating evolution. Importantly however, individual‐based simulations show that the correlation between fluctuating selection and fluctuating evolution can be obscured by the effect of drift, and that substantially more data are required for a precise and accurate estimate of this correlation. We identify new challenges in measuring the coupling between selection and evolution, and provide methods and guidelines to overcome them.     

Body size effects and rates of cytochrome b evolution in tube-nosed seabirds

Variation in rates of molecular evolution now appears to be widespread. The demonstration that body size is correlated with rates of molecular evolution suggests that physiological and ecological factors may be involved in molecular rate variation, but large-scale comparative studies are still lacking. Here, we use complete cytochrome b sequences from 85 species of tube-nosed seabirds (order Procellariiformes) and 5 outgroup species of penguins (order Sphenisciformes) to test for an association between body mass and rates of molecular evolution within the former avian order. Cladistic analysis of the 90 sequences estimates a phylogeny largely consistent with the traditional taxonomy of the Procellariiformes. The Diomedeidae, Procellariidae, and Pelecanoididae are monophyletic, while the Hydrobatidae are basal and paraphyletic. However, the two subfamilies within the Hydrobatidae (Hydrobatinae and Oceanitinae) are monophyletic. A likelihood ratio test detects significant deviation from clocklike evolution in our data. Using a sign test for an association between body mass and branch length in the seabird phylogeny, we find that larger taxa tend to have shorter terminal branch lengths than smaller taxa. This observation suggests that rates of mitochondrial DNA evolution are slower for larger taxa. Rate calibrations based on the fossil record reveal concordant body size effects. We interpret these results as evidence for a metabolic rate effect, as the species in this order exhibit large differences in metabolic rates, which are known to be highly correlated with body mass in this group. Our results support previous findings of body size effects and show that this effect can be significant even within a single avian order. This suggests that even lineage-specific molecular clocks may not be tenable if calibrations involve taxa with different metabolic rates.      

The evolution of body size in extant groups of North American freshwater fishes: speciation,size distributions,and Cope's rule

Change in body size within an evolutionary lineage over time has been under investigation since the synthesis of Cope's rule, which suggested that there is a tendency for mammals to evolve larger body size. Data from the fossil record have subsequently been examined for several other taxonomic groups to determine whether they also displayed an evolutionary increase in body size. However, we are not aware of any species-level study that has investigated the evolution of body size within an extant continental group. Data acquired from the fossil record and data derived from the evolutionary relationships of extant species are not similar, with each set exhibiting both strengths and weaknesses related to inferring evolutionary patterns. Consequently, expectation that general trends exhibited in the fossil record will correspond to patterns in extant groups is not necessarily warranted. Using phylogenetic relationships of extant species, we show that five of nine families of North American freshwater fishes exhibit an evolutionary trend of decreasing body size. These trends result from the basal position of large species and the more derived position of small species within families. Such trends may be caused by the invasion of small streams and subsequent isolation and speciation. This pattern, potentially influenced by size-biased dispersal rates and the high percentage of small streams in North America, suggests a scenario that could result in the generation of the size-frequency distribution of North American freshwater fishes.     

Differential rates of morphological divergence in birds

There are more small-bodied bird species than there are large-bodied, even on a logarithmic scale. In birds this pattern, which is also found in other higher taxa, appears not to be due to neutral evolution. It has often been suggested that the skew of body size frequency distributions is the result of a relationship between body size and the net rate of speciation, but phylogenetic analyses so far have rejected the hypothesis that small-bodied species are subject to higher net rates of speciation. On the contrary, we show that there exists a relationship between body size and its own evolutionary variability: avian families of small body size show less interspecific variation in body size than large-bodied families of similar age and species richness.     

Larger brains spur species diversification in birds

Evidence is accumulating that species traits can spur their evolutionary diversification by influencing niche shifts, range expansions, and extinction risk. Previous work has shown that larger brains (relative to body size) facilitate niche shifts and range expansions by enhancing behavioral plasticity but whether larger brains also promote evolutionary diversification is currently backed by insufficient evidence. We addressed this gap by combining a brain size dataset for >1900 avian species worldwide with estimates of diversification rates based on two conceptually different phylogenetic‐based approaches. We found consistent evidence that lineages with larger brains (relative to body size) have diversified faster than lineages with relatively smaller brains. The best supported trait‐dependent model suggests that brain size primarily affects diversification rates by increasing speciation rather than decreasing extinction rates. In addition, we found that the effect of relatively brain size on species‐level diversification rate is additive to the effect of other intrinsic and extrinsic factors. Altogether, our results highlight the importance of brain size as an important factor in evolution and reinforce the view that intrinsic features of species have the potential to influence the pace of evolution.     

Body size evolution in Mesozoic birds: little evidence for Cope's rule

Cope's rule, the tendency towards evolutionary increases in body size, is a long-standing macroevolutionary generalization that has the potential to provide insights into directionality in evolution; however, both the definition and identification of Cope's rule are controversial and problematic. A recent study [J. Evol. Biol. 21 (2008) 618] examined body size evolution in Mesozoic birds, and claimed to have identified evidence of Cope's rule occurring as a result of among-lineage species sorting. We here reassess the results of this study, and additionally carry out novel analyses testing for within-lineage patterns in body size evolution in Mesozoic birds. We demonstrate that the nonphylogenetic methods used by this previous study cannot distinguish between among- and within-lineage processes, and that statistical support for their results and conclusions is extremely weak. Our ancestor-descendant within-lineage analyses explicitly incorporate recent phylogenetic hypotheses and find little compelling evidence for Cope's rule. Cope's rule is not supported in Mesozoic birds by the available data, and body size evolution currently provides no insights into avian survivorship through the Cretaceous-Paleogene mass extinction.     

Molecular clocks in reptiles: life history influences rate of molecular evolution

Life history has been implicated as a determinant of variation in rate of molecular evolution amongst vertebrate species because of a negative correlation between body size and substitution rate for many molecular data sets. Both the generality and the cause of the negative body size trend have been debated, and the validity of key studies has been questioned (particularly concerning the failure to account for phylogenetic bias). In this study, a comparative method has been used to test for an association between a range of life-history variables-such as body size, age at maturity, and clutch size-and DNA substitution rate for three genes (NADH4, cytochrome b, and c-mos). A negative relationship between body size and rate of molecular evolution was found for phylogenetically independent pairs of reptile species spanning turtles, lizards, snakes, crocodile, and tuatara. Although this study was limited by the number of comparisons for which both sequence and life-history data were available, the results suggest that a negative body size trend in rate of molecular evolution may be a general feature of reptile molecular evolution, consistent with similar studies of mammals and birds. This observation has important implications for uncovering the mechanisms of molecular evolution and warns against assuming that related lineages will share the same substitution rate (a local molecular clock) in order to date evolutionary divergences from DNA sequences.     

Macroecology and macroevolution of body size in Anolis lizards

Body size is one of the most influential traits affecting many ecological and physiological processes across animal and plant taxa. Studies of the environmental factors shaping body size patterns may evaluate either temporal or spatial dimensions. Here, we analyzed body size evolution in the radiation of Anolis lizards across both geographical and temporal dimensions. We used a set of macroecological and macroevolutionary methods to test current and past environmental effects on geographical gradients of body size and its evolutionary rates. First, we test whether a set of current ecological/physiological hypotheses (heat balance, productivity and seasonality) explains spatial body size gradients. Second, we evaluate how tempo (i.e. evolutionary rates) and mode (i.e. evolutionary process) of body size evolution changed through time and the role of paleo-temperatures on rates of body size evolution during the Cenozoic. We did not find a signature of current environmental variables driving spatial body size gradients. By contrast, we found strong support for a correlation between temperature changes (i.e. climate cooling) during the Cenozoic and rates of body size evolution (i.e. body size diversification). We suggest that patterns of body size evolution in Anolis lizards might be influenced by thermoregulatory behavior across clades and regions.     

Primate longevity: Its place in the mammalian scheme

Data on captive longevity in 587 mammalian species were analyzed in order to evaluate primate longevity in the context of general mammalian life history patterns. Contrary to some recurrent claims in the literature, we found that 1) primates are not the longest-lived mammalian order, either by absolute longevity, longevity corrected for body size, or metabolic expenditure per lifetime; 2) although relative brain size is highly correlated with longevity in primates, this is an aberrant trend for mammals in general, and other body organs account for an even greater amount of variation in longevity; and 3) there has been no progressive evolution of increased longevity among the primate superfamilies. The exceptional magnitude of primate longevity may, in keeping with evolutionary senescence theory, be due to an evolutionary history of low vulnerability to environmentally imposed death due to their body size, arboreal habit, and propensity to live in social groups. © 1992 Wiley-Liss, Inc.     

The geometry of taking flight: Limb morphometrics in Mesozoic theropods

Theropoda was one of the most successful dinosaurian clades during the Mesozoic and has remained a dominant component of faunas throughout the Cenozoic, with nearly 10,000 extant representatives. The discovery of Archaeopteryx provides evidence that avian theropods evolved at least 155 million years ago and that more than half of the tenure of avian theropods on Earth was during the Mesozoic. Considering the major changes in niche occupation for theropods resulting from the evolution of arboreal and flight capabilities, we have analyzed forelimb and hindlimb proportions among nonmaniraptoriform theropods, nonavian maniraptoriforms, and basal avialans using reduced major axis regressions, principal components analysis, canonical variates analysis, and discriminant function analysis. Our study is the first analysis on theropod limb proportions to apply phylogenetic independent contrasts and size corrections to the data to ensure that all the data are statistically independent and amenable to statistical analyses. The three ordination analyses we performed did not show any significant groupings or deviations between nonavian theropods and Mesozoic avian forms when including all limb elements. However, the bivariate regression analyses did show some significant trends between individual elements that suggested evolutionary trends of increased forelimb length relative to hindlimb length from nonmaniraptoriform theropods to nonavian maniraptoriforms to basal avialans. The increase in disparity and divergence away from the nonavian theropod body plan is well documented within Cenozoic forms. The lack of significant groupings among Mesozoic forms when examining the entire theropod body plan concurrently suggests that nonavian theropods and avian theropods did not substantially diverge in limb proportions until the Cenozoic. J. Morphol. 276:152–166, 2015. © 2014 Wiley Periodicals, Inc.     

Effects of allometry,productivity and lifestyle on rates and limits of body size evolution

Body size affects nearly all aspects of organismal biology, so it is important to understand the constraints and dynamics of body size evolution. Despite empirical work on the macroevolution and macroecology of minimum and maximum size, there is little general quantitative theory on rates and limits of body size evolution. We present a general theory that integrates individual productivity, the lifestyle component of the slow–fast life-history continuum, and the allometric scaling of generation time to predict a clade''s evolutionary rate and asymptotic maximum body size, and the shape of macroevolutionary trajectories during diversifying phases of size evolution. We evaluate this theory using data on the evolution of clade maximum body sizes in mammals during the Cenozoic. As predicted, clade evolutionary rates and asymptotic maximum sizes are larger in more productive clades (e.g. baleen whales), which represent the fast end of the slow–fast lifestyle continuum, and smaller in less productive clades (e.g. primates). The allometric scaling exponent for generation time fundamentally alters the shape of evolutionary trajectories, so allometric effects should be accounted for in models of phenotypic evolution and interpretations of macroevolutionary body size patterns. This work highlights the intimate interplay between the macroecological and macroevolutionary dynamics underlying the generation and maintenance of morphological diversity.     

BODY AND LIMB SIZE DISSOCIATION AT THE ORIGIN OF BIRDS: UNCOUPLING ALLOMETRIC CONSTRAINTS ACROSS A MACROEVOLUTIONARY TRANSITION

The origin of birds and powered flight is a classic major evolutionary transition. Research on their origin often focuses on the evolution of the wing with trends of forelimb elongation traced back through many nonavian maniraptoran dinosaurs. We present evidence that the relative forelimb elongation within avian antecedents is primarily due to allometry and is instead driven by a reduction in body size. Once body size is factored out, there is no trend of increasing forelimb length until the origin of birds. We report that early birds and nonavian theropods have significantly different scaling relationships within the forelimb and hindlimb skeleton. Ancestral forelimb and hindlimb allometric scaling to body size is rapidly decoupled at the origin of birds, when wings significantly elongate, by evolving a positive allometric relationship with body size from an ancestrally negative allometric pattern and legs significantly shorten by keeping a similar, near isometric relationship but with a reduced intercept. These results have implications for the evolution of powered flight and early diversification of birds. They suggest that their limb lengths first had to be dissociated from general body size scaling before expanding to the wide range of fore and hindlimb shapes and sizes present in today's birds.     

Size increase and form allometry during evolution of ciliate species in the genera Colpoda and Tillina (Ciliophora: Colpodida).

With the absence of a fossil record to provide direct evidence of evolutionary relationships, many researchers have inferred by circular reasoning that body size increase and form allometry have occurred during the evolution of ciliated protozoa. This study establishes ancestor-descendant relationships among five species of the related genera Colpoda and Tillina using ultrastructural characteristics which are not apparently dependent on size and form. This independent test suggests that phylogenetic size increase and phylogenetic form allometry have occurred during the evolution of these ciliates. Interrelationships of body size increase, increase in number of cortical organelles, and form allometry are discussed in reference to the divergence of these ciliate species.     

Ecological and Evolutionary Processes Drive the Origin and Maintenance of Imperfect Mimicry

Although the forces behind the evolution of imperfect mimicry remain poorly studied, recent hypotheses suggest that relaxed selection on small-bodied individuals leads to imperfect mimicry. While evolutionary history undoubtedly affects the development of imperfect mimicry, ecological community context has largely been ignored and may be an important driver of imperfect mimicry. Here we investigate how evolutionary and ecological contexts might influence mimetic fidelity in Müllerian and Batesian mimicry systems. In Batesian hoverfly systems we find that body size is not a strong predictor of mimetic fidelity. However, in Müllerian velvet ants we find a weak positive relationship between body size and mimetic fidelity when evolutionary context is controlled for and a much stronger relationship between community diversity and mimetic fidelity. These results suggest that reduced selection on small-bodied individuals may not be a major driver of the evolution of imperfect mimicry and that other factors, such as ecological community context, should be considered when studying the evolution of imperfect mimicry.     

Body size evolution in Mesozoic birds

The tendency for the mean body size of taxa within a clade to increase through evolution (Cope's Rule) has been demonstrated in a number of terrestrial vertebrate groups. However, because avian body size is strongly constrained by flight, any increase in size during the evolution of this lineage should be limited - there is a maximum size that can be attained by a bird for it to be able to get off the ground. Contrary to previous interpretations of early avian evolution, we demonstrate an overall increase in body size across Jurassic and Cretaceous flying birds: taxon body size increases from the earliest Jurassic through to the end of the Cretaceous, across a time span of 70 Myr. Although evidence is limited that this change is directional, it is certainly nonrandom. Relative size increase occurred presumably as the result of an increase in variance as the avian clade diversified after the origin of flight: a progression towards larger body size is seen clearly within the clades Pygostylia and Ornithothoraces. In contrast, a decrease in body size characterizes the most crownward lineage Ornithuromorpha, the clade that includes all extant taxa, and potentially may explain the survival of these birds across the Cretaceous-Palaeogene boundary. As in all other dinosaurs, counter selection for small size is seen in some clades, whereas body size is increasing overall.     

Air‐filled postcranial bones in theropod dinosaurs: physiological implications and the ‘reptile’–bird transition

Pneumatic (air‐filled) postcranial bones are unique to birds among extant tetrapods. Unambiguous skeletal correlates of postcranial pneumaticity first appeared in the Late Triassic (approximately 210 million years ago), when they evolved independently in several groups of bird‐line archosaurs (ornithodirans). These include the theropod dinosaurs (of which birds are extant representatives), the pterosaurs, and sauropodomorph dinosaurs. Postulated functions of skeletal pneumatisation include weight reduction in large‐bodied or flying taxa, and density reduction resulting in energetic savings during foraging and locomotion. However, the influence of these hypotheses on the early evolution of pneumaticity has not been studied in detail previously. We review recent work on the significance of pneumaticity for understanding the biology of extinct ornithodirans, and present detailed new data on the proportion of the skeleton that was pneumatised in 131 non‐avian theropods and Archaeopteryx. This includes all taxa known from significant postcranial remains. Pneumaticity of the cervical and anterior dorsal vertebrae occurred early in theropod evolution. This ‘common pattern’ was conserved on the line leading to birds, and is likely present in Archaeopteryx. Increases in skeletal pneumaticity occurred independently in as many as 12 lineages, highlighting a remarkably high number of parallel acquisitions of a bird‐like feature among non‐avian theropods. Using a quantitative comparative framework, we show that evolutionary increases in skeletal pneumaticity are significantly concentrated in lineages with large body size, suggesting that mass reduction in response to gravitational constraints at large body sizes influenced the early evolution of pneumaticity. However, the body size threshold for extensive pneumatisation is lower in theropod lineages more closely related to birds (maniraptorans). Thus, relaxation of the relationship between body size and pneumatisation preceded the origin of birds and cannot be explained as an adaptation for flight. We hypothesise that skeletal density modulation in small, non‐volant, maniraptorans resulted in energetic savings as part of a multi‐system response to increased metabolic demands. Acquisition of extensive postcranial pneumaticity in small‐bodied maniraptorans may indicate avian‐like high‐performance endothermy.     

Similarity of growth among Great tits (Parus major) and Blue tits (P. caeruleus)

Differences in morphology among species are proximately caused by changes in the ontogeny of individuals. It is therefore of importance to analyse possible differences in growth parameters among closely related species in order to understand what parameters are most and least likely, respectively, to change in evolution. In this paper I analyse growth in two closely related sympatric species, namely Great tit, Parus major, and Blue tit, P. caeruleus. The former is considerably larger than the latter in all external traits. The growth rates of the two species were found to be very similar for all traits, thus excluding differences in growth rate as a potential cause of evolutionary size changes. Offset of growth occurred at relatively similar times in the two species, excluding this factor as a major cause of the final size differences. However, size differences at hatching were pronounced and remained so throughout ontogeny, pointing to initial size (egg size or hatching size) as the target of factors promoting change. Bivariate allometric relations of traits vs. body size (mass) were similar between the two species at all ontogenetic stages. There was a high correlation among traits especially at intermediate age stages (5 and 8 days), but these correlations became weaker at older age and approached the low pattern of integration found in adults. All this suggests the operation of a general growth factor affecting all parts of the phenotype simultaneously, which has its major influence at the time of maximal growth. If closely related species in general have highly similar growth patterns, strong evolutionary allometry as found in many avian taxa is to be expected.     

Evolutionary basis of parallelism in North American scincid lizards

This study uses a phylogenetic framework to explore the causes of parallelism in two North American scincid lizard assemblages: the skiltonianus and fasciatus species groups of the genus Plestiodon. Each group consists of several closely related species with conserved neonate morphology; features that distinguish species become accentuated during ontogeny, and these differences often resemble different endpoints along a developmental continuum. This continuum is believed to be an expression of the ancestral ontogeny, and has led to the hypothesis that evolutionary change in development has generated much of the observed morphological diversity. However, progress on understanding these mechanisms is limited by a lack of well-supported phylogenetic data for the fasciatus group, and for Plestiodon in general. Recent phylogenetic studies on the skiltonianus group have revealed previously undetected cases of parallelism, and raise the possibility that similar cases have yet to be discovered in the fasciatus group. Here, I estimate a phylogeny to test the monophyly of the fasciatus group and infer its relationship with other North American Plestiodon using 2537 bp from six mtDNA genes. I use the phylogeny to reconstruct the mode (graduated vs. punctuated) and direction of body size evolution, to map the evolution of two predominant color morphs, and to test whether size and color pattern evolve concertedly. The results show that the morphotypes of the traditional fasciatus group constitute good species, but that the species group is rendered paraphyletic by several geographically overlapping species that deviate from the fasciatus-like ontogeny. Body size evolution has occurred gradually and bi-directionally, and shifts to large body size have been consistently associated with the loss of the striped color pattern during ontogeny. I show that parallelism, a lack of rigorous phylogenetic analysis, and a reliance on shared ontogenetic features for predicting phylogenetic relatedness, has misled the traditional systematics of these lizards, but that general ideas concerning the role of development in their morphological evolution remain supported. I close by proposing that the processes influencing repeated phyletic patterns in the skiltonianus and fasciatus groups represent adherence to an ancestral ground state, and discuss the importance of using phylogenies for the initial characterization of evolutionary changes in development.     

Predicting evolution with generalized models of divergent selection: a case study with poeciliid fish

Over the past century and half since the process of natural selection was first described, one enduring question has captivated many, "how predictable is evolution?" Because natural selection comprises deterministic components, the course of evolution may exhibit some level of predictability across organismal groups. Here, I provide an early appraisal of the utility of one particular approach to understanding the predictability of evolution: generalized models of divergent selection (GMDS). The GMDS approach is meant to provide a unifying framework for the science of evolutionary prediction, offering a means of better understanding the causes and consequences of phenotypic and genetic evolution. I describe and test a GMDS centered on the evolution of body shape, size of the gonopodium (sperm-transfer organ), steady-swimming abilities, fast-start swimming performance, and reproductive isolation between populations in Gambusia fishes (Family Poeciliidae). The GMDS produced some accurate evolutionary predictions in Gambusia, identifying variation in intensity of predation by piscivorous fish as a major factor driving repeatable and predictable phenotypic divergence, and apparently playing a key role in promoting ecological speciation. Moreover, the model's applicability seems quite general, as patterns of differentiation in body shape between predator regimes in many disparate fishes match the model's predictions. The fact that such a simple model could yield accurate evolutionary predictions in distantly related fishes inhabiting different geographic regions and types of habitat, and experiencing different predator species, suggests that the model pinpointed a causal factor underlying major, shared patterns of diversification. The GMDS approach appears to represent a promising method of addressing the predictability of evolution and identifying environmental factors responsible for driving major patterns of replicated evolution.     

Size-assortative mating and sexual size dimorphism are predictable from simple mechanics of mate-grasping behavior

Background  

A major challenge in evolutionary biology is to understand the typically complex interactions between diverse counter-balancing factors of Darwinian selection for size assortative mating and sexual size dimorphism. It appears that rarely a simple mechanism could provide a major explanation of these phenomena. Mechanics of behaviors can predict animal morphology, such like adaptations to locomotion in animals from various of taxa, but its potential to predict size-assortative mating and its evolutionary consequences has been less explored. Mate-grasping by males, using specialized adaptive morphologies of their forelegs, midlegs or even antennae wrapped around female body at specific locations, is a general mating strategy of many animals, but the contribution of the mechanics of this wide-spread behavior to the evolution of mating behavior and sexual size dimorphism has been largely ignored.