CONVERGENT EVOLUTION OF SEXUAL DIMORPHISM IN SKULL SHAPE USING DISTINCT DEVELOPMENTAL STRATEGIES

Studies integrating evolutionary and developmental analyses of morphological variation are of growing interest to biologists as they promise to shed fresh light on the mechanisms of morphological diversification. Sexually dimorphic traits tend to be incredibly divergent across taxa. Such diversification must arise through evolutionary modifications to sex differences during development. Nevertheless, few studies of dimorphism have attempted to synthesize evolutionary and developmental perspectives. Using geometric morphometric analysis of head shape for 50 Anolis species, we show that two clades have converged on extreme levels of sexual dimorphism through similar, male‐specific changes in facial morphology. In both clades, males have evolved highly elongate faces whereas females retain faces of more moderate proportion. This convergence is accomplished using distinct developmental mechanisms; one clade evolved extreme dimorphism through the exaggeration of a widely shared, potentially ancestral, developmental strategy whereas the other clade evolved a novel developmental strategy not observed elsewhere in the genus. Together, our analyses indicate that both shared and derived features of development contribute to macroevolutionary patterns of morphological diversity among Anolis lizards.     

COMPUTER-SIMULATED SHELL SIZE AND SHAPE VARIATION IN THE CARIBBEAN LAND SNAIL GENUS CERION: A TEST OF GEOMETRICAL CONSTRAINTS

A computer graphical model of gastropod shell form is used to test a hypothesis of geometric constraint proposed to explain the disjunct distribution of shell forms observed in Cerion, a species-rich and geometrically varied genus of terrestrial gastropods. The mapping of computer-simulated forms into a morphospace of Cerion shells produces a continuum of sizes and shapes. Therefore, the absence of particular shell forms is not explained by geometric constraints. Two proposed modes of shell morphogenesis at extreme ranges in size (“dwarfs” and “giants”) previously were thought to be exclusive routes to the construction of high-spired (“smokestack”) forms. The present study shows that there are, in fact, multiple routes of transformation. In addition, these routes are geometrically reversible and interconnect the members of the shell-form continuum. Thus, the possible pathways followed during the course of evolution within this genus cannot be determined until an adequate phylogenetic hypothesis has been proposed.     

MORPHOLOGICAL RATES OF ANGIOSPERM SEED SIZE EVOLUTION

The evolution of seed size among angiosperms reflects their ecological diversification in a complex fitness landscape of life‐history strategies. The lineages that have evolved seeds beyond the upper and lower boundaries that defined nonflowering seed plants since the Paleozoic are more dispersed across the angiosperm phylogeny than would be expected under a neutral model of phenotypic evolution. Morphological rates of seed size evolution estimated for 40 clades based on 17,375 species ranged from 0.001 (Garryales) to 0.207 (Malvales). Comparative phylogenetic analysis indicated that morphological rates are not associated with the clade's seed size but are negatively correlated with the clade's position in the overall distribution of angiosperm seed sizes; clades with seed sizes closer to the angiosperm mean had significantly higher morphological rates than clades with extremely small or extremely large seeds. Likewise, per‐clade taxonomic diversification rates are not associated with the seed size of the clade but with where the clade falls within the angiosperm seed size distribution. These results suggest that evolutionary rates (morphological and taxonomic) are elevated in densely occupied regions of the seed morphospace relative to lineages whose ecophenotypic innovations have moved them toward the edges.     

THE ROLE OF GRAVITY IN THE EVOLUTION OF MAMMALIAN BLOOD PRESSURE

Understanding of the factors involved in determining the level of central arterial blood pressure in mammals has been clouded by inappropriate allometric analyses that fail to account for phylogenetic relationships among species, and require pressure to approach 0 as body size decreases. The present study analyses systolic, mean arterial, and diastolic blood pressure in 47 species of mammal with phylogenetically informed techniques applied to two‐parameter equations. It also sets nonlinear, three‐parameter equations to the data to remove the assumption of the two‐parameter power equation that the smallest animals must have negligible blood pressure. These analyses show that blood pressure increases with body size. Nonlinear analyses show that mean blood pressure increases from 93 mmHg in a 10 g mouse to 156 mmHg in a 4 tonne elephant. The scaling exponent of blood pressure is generally lower than, though not significantly different from, the exponent predicted on the basis of the expected scaling of the vertical distance between the head and the heart. This indicates that compensation for the vertical distance above the heart is not perfect and suggests that the pressure required to perfuse the capillaries at the top of the body may decrease in larger species.     

LIFE HISTORY AND THE EVOLUTION OF PARENTAL CARE

Patterns of parental care are strikingly diverse in nature, and parental care is thought to have evolved repeatedly multiple times. Surprisingly, relatively little is known about the most general conditions that lead to the origin of parental care. Here, we use a theoretical approach to explore the basic life‐history conditions (i.e., stage‐specific mortality and maturation rates, reproductive rates) that are most likely to favor the evolution of some form of parental care from a state of no care. We focus on parental care of eggs and eggs and juveniles and consider varying magnitudes of the benefits of care. Our results suggest that parental care can evolve under a range of life‐history conditions, but in general will be most strongly favored when egg death rate in the absence of care is high, juvenile survival in the absence of care is low (for the scenario in which care extends into the juvenile stage), adult death rate is relatively high, egg maturation rate is low, and the duration of the juvenile stage is relatively short. Additionally, parental care has the potential to be favored at a broad range of adult reproductive rates. The relative importance of these life‐history conditions in favoring or limiting the evolution of care depends on the magnitude of the benefits of care, the relationship between initial egg allocation and subsequent offspring survival, and whether care extends into the juvenile stage. The results of our model provide a general set of predictions regarding when we would expect parental care to evolve from a state of no care, and in conjunction with other work on the topic, will enhance our understanding of the evolutionary dynamics of parental care and facilitate comparative analyses.     

SIZE‐FECUNDITY RELATIONSHIPS,GROWTH TRAJECTORIES,AND THE TEMPERATURE‐SIZE RULE FOR ECTOTHERMS

Many ectotherms show crossing growth trajectories as a plastic response to rearing temperature. As a result, individuals growing up in cool conditions grow slower, mature later, but are larger at maturation than those growing up in warm conditions. To date, no entirely satisfactory explanation has been found for why this pattern, often called the temperature‐size rule, should exist. Previous theoretical models have assumed that size‐specific mortality rates were most likely to drive the pattern. Here, I extend one theoretical model to show that variation in size‐fecundity relationships may also be important. Plasticity in the size‐fecundity relationship has rarely been considered, but a number of studies show that fecundity increases more quickly with size in cold environments than it does in warm environments. The greater increase in fecundity offsets costs of delayed maturation in cold environments, favoring a larger size at maturation. This can explain many cases of crossing growth trajectories, not just in relation to temperature.     

ONE SIZE FITS ALL? RELATIONSHIPS BETWEEN THE SIZE AND DEGREE OF VARIATION IN GENITALIA AND OTHER BODY PARTS IN TWENTY SPECIES OF INSECTS AND SPIDERS

Hypotheses regarding the function of elaborate male genitalia were tested in a sample of insects and spiders by comparing their allometric values (slopes in log-log regressions on indicators of body size) with those of other body parts. Male genitalia consistently had lower slopes than other body parts. Perhaps as a consequence of this pattern, genitalic size also tended, though less consistently, to have lower coefficients of variation than did the size of other body parts. The morphological details of coupling between males and females in several species clearly indicated that selection favoring mechanical fit is not responsible for these trends. Sexual selection on male courtship structures that are brought into contact with females in precise ways may favor relatively low allometric values, in contrast to the high values seen in the other sexually selected characters (usually visual display devices) that have been studied previously, because a female's own size will influence her perception of the contact courtship devices of a male.     

THE EVOLUTION OF INDIVIDUAL VARIATION IN COMMUNICATION STRATEGIES

Communication is a process in which senders provide information via signals and receivers respond accordingly. This process relies on two coevolving conventions: a “sender code” that determines what kind of signal is to be sent given the sender's state; and a “receiver code” that determines the appropriate responses to different signal types. By means of a simple but generic model, we show that polymorphic sender and receiver strategies emerge naturally during the evolution of communication, and that the number of alternative strategies observed at equilibrium depends on the potential for error in signal production. Our model suggests that alternative communication strategies will evolve whenever senders possess imperfect information about their own quality or state, signals are costly, and genetic mechanisms allow for a correlation between sender and receiver behavior. These findings provide an explanation for recent reports of individual differences in communication strategies, and suggest that the amount of individual variation that can be expected in communication systems depends on the type of information being conveyed. Our model also suggests a link between communication and the evolution of animal personalities, which is that individual differences in the production and interpretation of signals can result in consistent differences in behavior.     

EXTINCTIONS IN HETEROGENEOUS ENVIRONMENTS AND THE EVOLUTION OF MODULARITY

Extinctions of local subpopulations are common events in nature. Here, we ask whether such extinctions can affect the design of biological networks within organisms over evolutionary timescales. We study the impact of extinction events on modularity of biological systems, a common architectural principle found on multiple scales in biology. As a model system, we use networks that evolve toward goals specified as desired input–output relationships. We use an extinction–recolonization model, in which metapopulations occupy and migrate between different localities. Each locality displays a different environmental condition (goal), but shares the same set of subgoals with other localities. We find that in the absence of extinction events, the evolved computational networks are typically highly optimal for their localities with a nonmodular structure. In contrast, when local populations go extinct from time to time, we find that the evolved networks are modular in structure. Modular circuitry is selected because of its ability to adapt rapidly to the conditions of the free niche following an extinction event. This rapid adaptation is mainly achieved through genetic recombination of modules between immigrants from neighboring local populations. This study suggests, therefore, that extinctions in heterogeneous environments promote the evolution of modular biological network structure, allowing local populations to effectively recombine their modules to recolonize niches.     

TUNING A GENETIC SWITCH: EXPERIMENTAL EVOLUTION AND NATURAL VARIATION OF PROPHAGE INDUCTION

Genetic switches allow organisms to modulate their phenotype in response to environmental changes. Understanding the evolutionary processes by which switches are tuned is central to understanding how phenotypic variation is realized. Prophage induction by phage λ is the classic example of a genetic switch and allows λ to move between two different modes of transmission: as a lysogen it reproduces vertically as a component of the host genome; as a free phage it reproduces horizontally by infectious epidemic spread. We show that the λ switch can respond rapidly to selection for alteration in sensitivity and threshold. Sequencing of candidate genes in the genetic circuitry underlying the switch revealed mutations of likely adaptive significance in some, but not all candidates, suggesting that the core genetic circuitry plays a limited role in the fine‐tuning of the switch in vivo. The relative ease with which the switch could be tuned by selection was further indicated by extensive variation in sensitivity and threshold of its response function among wild lambdoid phages. Together, our findings emphasize the adaptive significance of a finely tuned switch and draw attention to the selective factors shaping prophage induction in natural phage populations.     

NATURAL GENETIC VARIATION OF LIFE SPAN,REPRODUCTION, AND JUVENILE GROWTH IN DAPHNIA

The evolutionary theory of senescence predicts that high extrinsic mortality in natural populations should select for accelerated reproductive investment and shortened life span. Here, we test the theory with natural populations of the Daphnia pulex-pulicaria species complex, a group of freshwater zooplankton that spans an environmental gradient of habitat permanence. We document substantial genetic variation in demographic life-history traits among parent and hybrid populations of this complex. Populations from temporary ponds have shorter life spans, earlier and faster increases of intrinsic mortality risk, and earlier and steeper declines in fecundity than populations from permanent lakes. We also examine the age-specific contribution to fitness, measured by reproductive value, and to expected lifetime reproduction; these traits decline faster in populations from temporary ponds. Despite having more rapid senescence, pond Daphnia exhibit faster juvenile growth and higher early fitness, measured as population growth rate (r). Among populations within this species complex we observed negative genetic correlations between r and indices of life-history timing, suggesting trade-offs between early- and late-life performance. Our results cannot be explained by a trade-off between survival and fecundity or by nonevolutionary theories of senescence. Instead, our data are consistent with the evolutionary theory of senescence because the genetic variation in life histories we observed is roughly congruent with the temporal scale of environmental change in the field.     

INTERSPECIFIC COMPETITION ALTERS NONLINEAR SELECTION ON OFFSPRING SIZE IN THE FIELD

Offspring size is one of the most important life‐history traits with consequences for both the ecology and evolution of most organisms. Surprisingly, formal estimates of selection on offspring size are rare, and the degree to which selection (particularly nonlinear selection) varies among environments remains poorly explored. We estimate linear and nonlinear selection on offspring size, module size, and senescence rate for a sessile marine invertebrate in the field under three different intensities of interspecific competition. The intensity of competition strongly modified the strength and form of selection acting on offspring size. We found evidence for differences in nonlinear selection across the three environments. Our results suggest that the fitness returns of a given offspring size depend simultaneously on their environmental context, and on the context of other offspring traits. Offspring size effects can be more pervasive with regards to their influence on the fitness returns of other traits than previously recognized, and we suggest that the evolution of offspring size cannot be understood in isolation from other traits. Overall, variability in the form and strength of selection on offspring size in nature may reduce the efficacy of selection on offspring size and maintain variation in this trait.     

SHORT-TERM EVOLUTION IN THE SIZE AND SHAPE OF PEA APHIDS

Phenotypic evolution in contemporary populations can generally be witnessed only when novel selective forces produce rapid evolution. Examples of conditions that have led to rapid evolution include drastic environmental change, invasion of a new predator, or a host-range expansion. In cyclical parthenogens, however, yearly cycles of phenotypic evolution may occur due to the loss of adaptation during recombination in the sexual phase (genetic slippage), permitting an opportunity to observe adaptive evolutionary change in contemporary populations that are not necessarily subject to new patterns of natural selection. In insect herbivores, comparative studies suggest that morphological features that aid individuals in remaining on the plant or exploiting it as a food source are likely targets for selection. Here, we estimated the genetic variability of morphological traits in a cyclical parthenogen, the pea aphid (Acyrthosiphon pisum), to determine the potential for their evolution and we tested the hypothesis that size and/or shape evolves by clonal selection during one season of parthenogenetic reproduction. Genetic variation in a set of morphological traits was estimated using laboratory-reared descendents of clones collected from a single alfalfa field in May 1988 and April 1989 (henceforth, the “early” collections). In both years, there was significant clonal heritability early in the season both for overall morphology and for several individual aspects of size and shape. Because the course of short-term evolutionary change in the multivariate phenotype is a function of patterns of genetic covariance among characters, genetic correlations between size and 12 shape variables were also estimated for these early collections. A comparison between the mean phenotype of each early collection and that of a corresponding “late” collection made from the same field seven to eight clonal generations later in the same years revealed qualitatively similar changes in the average multivariate morphological phenotypes between the time periods in both years, although the difference was only significant for the 1989 samples. The pattern of genetic correlations that we estimated early in the 1989 season between overall size and various shape variables suggests that the observed short-term evolutionary changes in shape could have been due to natural selection acting only to increase overall size. We tested this hypothesis by estimating selection on size using a separate data set in which both demographic and morphological variables were measured on individuals reared under field conditions. Highly significant regressions of individual relative fitness on size were found for two major fitness components. Thus, it is likely that the evolutionary change in morphology that we observed is attributable to natural selection, possibly acting primarily through body size. A shift back to smaller size between the late 1988 and early 1989 collections from the same field suggests that either a cost of recombination or opposing selective forces during overwintering may produce persistent yearly cycles of morphological evolution in this cyclically parthenogenetic species.     

LOCAL ADAPTATION AND THE EVOLUTION OF PHENOTYPIC PLASTICITY IN TRINIDADIAN GUPPIES (POECILIA RETICULATA)

Divergent selection pressures across environments can result in phenotypic differentiation that is due to local adaptation, phenotypic plasticity, or both. Trinidadian guppies exhibit local adaptation to the presence or absence of predators, but the degree to which predator‐induced plasticity contributes to population differentiation is less clear. We conducted common garden experiments on guppies obtained from two drainages containing populations adapted to high‐ and low‐predation environments. We reared full‐siblings from all populations in treatments simulating the presumed ancestral (predator cues present) and derived (predator cues absent) conditions and measured water column use, head morphology, and size at maturity. When reared in presence of predator cues, all populations had phenotypes that were typical of a high‐predation ecotype. However, when reared in the absence of predator cues, guppies from high‐ and low‐predation regimes differed in head morphology and size at maturity; the qualitative nature of these differences corresponded to those that characterize adaptive phenotypes in high‐ versus low‐predation environments. Thus, divergence in plasticity is due to phenotypic differences between high‐ and low‐predation populations when reared in the absence of predator cues. These results suggest that plasticity might initially play an important role during colonization of novel environments, and then evolve as a by‐product of adaptation to the derived environment.     

ADAPTIVE PHENOTYPIC PLASTICITY IN GROWTH,DEVELOPMENT, AND BODY SIZE IN THE YELLOW DUNG FLY

Life-history theory predicts that age and size at maturity of organisms should be influenced by time and food constraints on development. This study investigated phenotypic plasticity in growth, development, body size, and diapause in the yellow dung fly, Scathophaga stercoraria. Full-sib families were allowed to develop under predator-free field conditions. The time before the onset of winter was varied and each brood was split into three environments differing in the amount of dung a set number of larvae had as a resource. When resources were abundant and competition was minimal, individuals of both sexes grew to larger body sizes, took longer time to mature, and were able to increase their growth rates to attain large body sizes despite shorter effective development periods later in the season. In contrast, limited larval resources and strong competition constrained individuals to mature earlier at a smaller adult size, and growth rates could not be increased but were at least maintained. This outcome is predicted by only two life-history optimality models, which treat mortality due to long development periods and mortality due to fast growth as independent. Elevated preadult mortality indicated physiological costs of fast growth independent of predation. When larval resources were limited, mortality increased with heritable variation in development time for males, and toward the end of the season mortality increased as larval resources became more abundant because this induced longer development periods. Sexual and fecundity selection favoring large body size in this species is thus opposed by larval viability selection favoring slower growth in general and shorter development periods when time and resources are limited; this overall combination of selective pressures is presumably shaping the reaction norms obtained here. Flexible growth rates are facilitated by low genetic correlations between development time and body size, a possible consequence of selection for plasticity. Heritable variation was evident in all traits investigated, as well as in phenotypic plasticity of these traits (genotype X interactions). This is possibly maintained by unpredictable spatiotemporal variation in dung abundance, competition, and hence selection.     

FITNESS CONSEQUENCES OF VARIATION IN EGG SIZE AND FOOD ABUNDANCE IN BROOK TROUT SALVELINUS FONTINALIS

Relationships between egg size and juvenile survival in brook trout, Salvelinus fontinalis, were determined experimentally at two levels of food abundance and then incorporated into a model that related maternal fitness to egg size and food supply. Egg volume was positively correlated with juvenile size at hatching and size at yolk sac resorption but had no significant effect on embryonic survival or development time. Juvenile survival was linearly related to egg size throughout the first 50 days of exogenous feeding at high and low food levels. The effects of egg size and food abundance on juvenile survival were not additive. Decreased food abundance significantly increased mortality among the smallest eggs but had a negligible effect on the largest eggs. Model simulations indicate that maternal fitness is a curvilinear function of egg size and that food supply influences both the height and the shape of the function. The fitness functions provide empirical support for the hypothesis that selection favors an increase in offspring size with reductions in resource abundance.     

GENETIC VARIATION IN HIF SIGNALING UNDERLIES QUANTITATIVE VARIATION IN PHYSIOLOGICAL AND LIFE‐HISTORY TRAITS WITHIN LOWLAND BUTTERFLY POPULATIONS

Oxygen conductance to the tissues determines aerobic metabolic performance in most eukaryotes but has cost/benefit tradeoffs. Here we examine in lowland populations of a butterfly a genetic polymorphism affecting oxygen conductance via the hypoxia‐inducible factor (HIF) pathway, which senses intracellular oxygen and controls the development of oxygen delivery networks. Genetically distinct clades of Glanville fritillary (Melitaea cinxia) across a continental scale maintain, at intermediate frequencies, alleles in a metabolic enzyme (succinate dehydrogenase, SDH) that regulates HIF‐1α. One Sdhd allele was associated with reduced SDH activity rate, twofold greater cross‐sectional area of tracheoles in flight muscle, and better flight performance. Butterflies with less tracheal development had greater post‐flight hypoxia signaling, swollen & disrupted mitochondria, and accelerated aging of flight metabolic performance. Allelic associations with metabolic and aging phenotypes were replicated in samples from different clades. Experimentally elevated succinate in pupae increased the abundance of HIF‐1α and expression of genes responsive to HIF activation, including tracheal morphogenesis genes. These results indicate that the hypoxia inducible pathway, even in lowland populations, can be an important axis for genetic variation underlying intraspecific differences in oxygen delivery, physiological performance, and life history.     

SPATIAL AND TEMPORAL VARIATION IN SELECTION ON CORRELATED LIFE-HISTORY TRAITS AND PLANT SIZE IN CHAMAECRISTA FASCICULATA

Intraspecific studies of selection on multiple traits of a plant's life history provide insight as to how the composite life history of an organism evolves. Current understanding of selection on plant life-history traits is deficient in three important areas: 1) the effects of selection through correlated traits, 2) the effects of selection on a trait throughout the plant's lifetime, and 3) spatial and temporal variation in selection on plant life-history traits among populations and years. This study documents spatial and temporal variation in selection on three life-history and two morphological traits for two natural populations of Chamaecrista fasciculata, a native summer annual. Life-history and morphological traits (date of seedling emergence, size at establishment, size prior to reproduction, date of initial flowering, and date of initial fruit maturation) varied significantly between sites and/or years. Selection on traits varied either spatially, between sites and among transects within one site, or temporally, between years. In addition, life-history traits were phenotypically correlated among themselves and with morphological traits; correlations were generally constant over time and space. Indirect selection caused changes in means and variances in traits not under direct selection, but which were correlated with traits under selection. Selection on date of emergence varied in direction and magnitude among different life-cycle stages, while selection on other traits varied only in magnitude among life stages of the plant. This study documents the complexity of the selective process and the importance of considering multiple life stages and traits when studying the evolution of life-history traits.     

FEMALE PROMISCUITY AND MATERNALLY DEPENDENT OFFSPRING GROWTH RATES IN MAMMALS

Conflicts between family members are expected to influence the duration and intensity of parental care. In mammals, the majority of this care occurs as resource transfer from mothers to offspring during gestation and lactation. Mating systems can have a strong influence on the severity of familial conflict—where female promiscuity is prevalent, conflict is expected to be higher between family members, causing offspring to demand more resources. If offspring are capable of manipulating their mothers and receive resources in proportion to their demands, resource transfer should increase with elevated promiscuity. We tested this prediction, unexplored across mammals, using a comparative approach. The total durations of gestation and lactation were not related to testes mass, a reliable proxy of female promiscuity across taxa. Offspring growth during gestation, however, and weaning mass, were positively correlated with testes mass, suggesting that offspring gain resources from their mothers at faster rates when familial conflict is greater. During gestation, the relationship between offspring growth and testes mass was also related to placenta morphology, with a stronger relationship between testes mass and growth observed in species with a less invasive placenta. Familial conflict could have a pervasive influence on patterns of parental care in mammals.     

EVOLUTION OF VIVIPARITY: A PHYLOGENETIC TEST OF THE COLD‐CLIMATE HYPOTHESIS IN PHRYNOSOMATID LIZARDS

The evolution of viviparity is a key life‐history transition in vertebrates, but the selective forces favoring its evolution are not fully understood. With >100 origins of viviparity, squamate reptiles (lizards and snakes) are ideal for addressing this issue. Some evidence from field and laboratory studies supports the “cold‐climate” hypothesis, wherein viviparity provides an advantage in cold environments by allowing mothers to maintain higher temperatures for developing embryos. Surprisingly, the cold‐climate hypothesis has not been tested using both climatic data and phylogenetic comparative methods. Here, we investigate the evolution of viviparity in the lizard family Phrynosomatidae using GIS‐based environmental data, an extensive phylogeny (117 species), and recently developed comparative methods. We find significant relationships between viviparity and lower temperatures during the warmest (egg‐laying) season, strongly supporting the cold‐climate hypothesis. Remarkably, we also find that viviparity tends to evolve more frequently at tropical latitudes, despite its association with cooler climates. Our results help explain this and two related patterns that seemingly contradict the cold‐climate hypothesis: the presence of viviparous species restricted to low‐elevation tropical regions and the paucity of viviparous species at high latitudes. Finally, we examine whether viviparous taxa may be at higher risk of extinction from anthropogenic climate change.