Heterochronic developmental shift caused by thyroid hormone in larval sand dollars and its implications for phenotypic plasticity and the evolution of nonfeeding development

Recent work on a diverse array of echinoderm species has demonstrated, as is true in amphibians, that thyroid hormone (TH) accelerates development to metamorphosis. Interestingly, the feeding larvae of several species of sea urchins seem to obtain TH through their diet of planktonic algae (exogenous source), whereas nonfeeding larvae of the sand dollar Peronella japonica produce TH themselves (endogenous source). Here we examine the effects of TH (thyroxine) and a TH synthesis inhibitor (thiourea) on the development of Dendraster excentricus, a sand dollar with a feeding larva. We report reduced larval skeleton lengths and more rapid development of the juvenile rudiment in the exogenous TH treatments when compared to controls. Also, larvae treated with exogenous TH reached metamorphic competence faster at a significantly reduced juvenile size, representing the greatest reduction in juvenile size ever reported for an echinoid species with feeding larvae. These effects of TH on D. excentricus larval development are strikingly similar to the phenotypically plastic response of D. excentricus larvae reared under high food conditions. We hypothesize that exogenous (algae-derived) TH is the plasticity cue in echinoid larvae, and that the larvae use ingested TH levels as an indicator for larval nutrition, ultimately signaling the attainment of metamorphic competence. Furthermore, our experiments with the TH synthesis inhibitor thiourea indicate that D. excentricus larvae can produce some TH endogenously. Endogenous TH production might, therefore, be a shared feature among sand dollars, facilitating the evolution of nonfeeding larval development in that group. Mounting evidence on the effects of thyroid hormones in echinoderm development suggests life-history models need to incorporate metamorphic hormone effects and the evolution of metamorphic hormone production.     

How body size and development biased the direction of evolution in early amphibians

Evolutionary change does not proceed in every direction with equal probability. Evolutionary biases or constraints are limitations on the mode, direction and tempo of evolution. Early tetrapods provide interesting examples, especially Paleozoic and Mesozoic amphibians. (1) Body size had a strong impact on morphology and development in early amphibians, resulting in manifold convergences imposed by design limitations. Miniaturisation had similar effects in a wide range of Paleozoic tetrapods, which are consistent with observations on extant salamanders. Gigantism was a common feature of Triassic temnospondyls, correlating with slow developmental rates similar to those of gigantic salamanders and the convergent evolution of bone density. (2) Ontogeny imposes constraints on evolution by canalised (buffered) developmental sequences. In Paleozoic temnospondyls, ontogenetic trajectories evolved by several different modes (truncation of the trajectory, shifting of events or condensation of events). Metamorphosis is an extreme example of a condensed developmental sequence, which first evolved in Paleozoic temnospondyls, increased in salamanders and culminated in anurans. It imposes strong biases that may be broken by three conceivable modes: (1) loss of the adult period (neoteny), (2) loss of the larval period (direct development) and (3) ‘unpacking’ of metamorphosis by re-evolving the plesiomorphic trajectory.     

Development of the nasal chemosensory organs in two terrestrial anurans: the directly developing frog, Eleutherodactylus coqui (Anura: Leptodactylidae), and the metamorphosing toad, Bufo americanus (Anura: Bufonidae)

Nearly all vertebrates possess an olfactory organ but the vomeronasal organ is a synapomorphy for tetrapods. Nevertheless, it has been lost in several groups of tetrapods, including aquatic and marine animals. The present study examines the development of the olfactory and vomeronasal organs in two terrestrial anurans that exhibit different developmental modes. This study compares the development of the olfactory and vomeronasal organs in metamorphic anurans that exhibit an aquatic larva (Bufo americanus) and directly developing anurans that have eliminated the tadpole (Eleutherodactylus coqui). The olfactory epithelium in larval B. americanus is divided into dorsal and ventral branches in the rostral and mid-nasal regions. The larval olfactory pattern in E. coqui has been eliminated. Ontogeny of the olfactory system in E. coqui embryos starts to vary substantially from the larval pattern around the time of operculum development, the temporal period when the larval stage is hypothesized to have been eliminated. The nasal anatomy of the two frogs does not appear morphologically similar until the late stages of embryogenesis in E. coqui and the terminal portion of metamorphosis in B. americanus. Both species and their respective developing offspring, aquatic tadpoles and terrestrial egg/embryos, possess a vomeronasal organ. The vomeronasal organ develops at mid-embryogenesis in E. coqui and during the middle of the larval period in B. americanus, which is relatively late for neobatrachians. Development of the vomeronasal organ in both frogs is linked to the developmental pattern of the olfactory system. This study supports the hypothesis that the most recent common ancestor of tetrapods possessed a vomeronasal organ and was aquatic, and that the vomeronasal organ was retained in the Amphibia, but lost in some other groups of tetrapods, including aquatic and marine animals.     

Geographic variation in clutch size and a realized benefit of aggregative feeding

We investigated one causal explanation for geographic variation in clutch size and aggregative feeding of the pipevine swallowtail, Battus philenor. Populations in California lay larger clutches than those in Texas, and larger feeding aggregations grow at an accelerated rate on the California host plant. Using reciprocal transplant experiments with larvae from California and Texas populations, we found that the benefit of increased growth rate associated with feeding in larger groups occurred only on the California host plant and was observed for larvae from both populations. These results are consistent with the hypothesis that larger clutch size and aggregative feeding are adaptations to characteristics of the California host plant. Future studies on the evolution of clutch size and aggregative feeding of herbivorous insects should consider how these life-history traits affect host plant suitability.     

Anatomical features of Leiopelma embryos and larvae: implications for anuran evolution

A controversial issue in anuran systematics is the relationship of Leiopelma to other anurans because recent phylogenetic constructions imply different relationships among the basal frogs. Of particular evolutionary interest is whether early development of Leiopelma resembles an ancestral salamander-like larva, an anuran tadpole, or neither. In the 1950s, Neville G. Stephenson hypothesized that direct development is the primary mode of development in amphibians, based on the fact that Leiopelma spp. lack a free-living (=feeding) larval stage. Although this hypothesis has not been generally accepted, it has not been formally refuted. We review Stephenson's work on Leiopelma and examine the anatomy of embryos/"larvae" of the four extant Leiopelma species for evidence of vestigial larval features that might refute the "direct-developing ancestor" hypothesis. We describe internal oral features in early developmental stages of Leiopelma and compare Leiopelma with a closely related basal anuran, Ascaphus, to assess whether their early developmental stages share any derived features. In Leiopelma hochstetteri, embryos/larvae have open gill slits and some faint rugosities around one gill slit that may be vestiges of gill rakers or filters. They also have more intestinal loops, indicative of an elongated alimentary tract, at earlier rather than late embryonic/larval stages. Collectively, these features support the view that the ancestor of Leiopelma had a free-swimming, free-feeding, aquatic larva. The palatoquadrate of Leiopelma archeyi reorients approximately 40 degrees from a more horizontal to a more vertical position through embryonic/"larval" development. This amount of cranial remodeling is intermediate between that seen in salamanders (17-27 degrees) and that reported for Ascaphus (64 degrees ) and other basal frogs (71-78 degrees) at metamorphosis. We found no internal oral features that Leiopelma shares specifically with Ascaphus. However, Leiopelma embryos have a ventrally positioned mouth and a downturned rostrum, characteristic of Ascaphus and other stream-adapted tadpoles.     

The evolution of coexistence: Reciprocal adaptation promotes the assembly of a simple community

Species coexistence may result by chance when co‐occurring species do not strongly interact or it may be an evolutionary outcome of strongly interacting species adapting to each other. Although patterns like character displacement indicate that coexistence has often been an evolutionary outcome, it is unclear how often the evolution of coexistence represents adaptation in only one species or reciprocal adaptation among all interacting species. Here, we demonstrate a strong role for evolution in the coexistence of guppies and killifish in Trinidadian streams. We experimentally recreated the temporal stages in the invasion and establishment of guppies into communities that previously contained only killifish. We combined demographic responses of guppies and killifish with a size‐based integral projection model to calculate the fitness of the phenotypes of each species in each of the stages of community assembly. We show that guppies from locally adapted populations that are sympatric with killifish have higher fitness when paired with killifish than guppies from allopatric populations. This elevated fitness involves effects traceable to both guppy and killifish evolution. We discuss the implications of our results to the study of species coexistence and how it may be mediated through eco‐evolutionary feedbacks.     

Pathogen-induced rapid evolution in a vertebrate life-history trait

Anthropogenic factors, including climate warming, are increasing the incidence and prevalence of infectious diseases worldwide. Infectious diseases caused by pathogenic parasites can have severe impacts on host survival, thereby altering the selection regime and inducing evolutionary responses in their hosts. Knowledge about such evolutionary consequences in natural populations is critical to mitigate potential ecological and economic effects. However, studies on pathogen-induced trait changes are scarce and the pace of evolutionary change is largely unknown, particularly in vertebrates. Here, we use a time series from long-term monitoring of perch to estimate temporal trends in the maturation schedule before and after a severe pathogen outbreak. We show that the disease induced a phenotypic change from a previously increasing to a decreasing size at maturation, the most important life-history transition in animals. Evolutionary rates imposed by the pathogen were high and comparable to those reported for populations exposed to intense human harvesting. Pathogens thus represent highly potent drivers of adaptive phenotypic evolution in vertebrates.     

Egg size evolution in tropical American arcid bivalves: the comparative method and the fossil record

Marine organisms exhibit a wide range of egg sizes, even among closely related taxa, and egg size is widely considered to be one of the most important components of the life histories of marine species. The nature of the trade-off between egg size and number and the consequences of variation in egg size for offspring growth and survivorship have been extensively modeled. Yet, there is little empirical evidence that supports the relative importance of particular environmental parameters in engendering the tremendous variation in egg size seen in marine organisms. This study compares egg sizes between six geminate species pairs of bivalves in the family Arcidae to determine whether egg size differs in predictable directions between geminate species in the two oceans separated by the Central American isthmus, and whether the direction and timing of egg size evolution among geminates in this family is correlated with both modern and paleoceanographic patterns of oceanic productivity. In all modern members of six geminate pairs, egg size was larger in the species in the western Atlantic than in its sister species the eastern Pacific. This pattern supports the hypothesis that optimal egg size differs in the two oceans due to the low productivity and poor larval feeding environment in the western Atlantic relative to the eastern Pacific. The fossil record of one geminate pair shows that egg size has remained consistently large in the western Atlantic from the Miocene to the Recent, while egg size in the eastern Pacific has decreased to the current small size in less than 2 million years; this suggests that modern-day differences between egg sizes in the western Atlantic and eastern Pacific are due to either an increase in productivity in the eastern Pacific and subsequent selection for smaller eggs in that ocean, or differential patterns of extinction that occurred well after the rise of the isthmus. These results agree with ancestral character state reconstruction using linear parsimony, but differ from squared-change parsimony reconstructions.     

Adaptation of Escherichia coli to glucose promotes evolvability in lactose

The selective history of a population can influence its subsequent evolution, an effect known as historical contingency. We previously observed that five of six replicate populations that were evolved in a glucose‐limited environment for 2000 generations, then switched to lactose for 1000 generations, had higher fitness increases in lactose than populations started directly from the ancestor. To test if selection in glucose systematically increased lactose evolvability, we started 12 replay populations—six from a population subsample and six from a single randomly selected clone—from each of the six glucose‐evolved founder populations. These replay populations and 18 ancestral populations were evolved for 1000 generations in a lactose‐limited environment. We found that replay populations were initially slightly less fit in lactose than the ancestor, but were more evolvable, in that they increased in fitness at a faster rate and to higher levels. This result indicates that evolution in the glucose environment resulted in genetic changes that increased the potential of genotypes to adapt to lactose. Genome sequencing identified four genes—iclR, nadR, spoT, and rbs—that were mutated in most glucose‐evolved clones and are candidates for mediating increased evolvability. Our results demonstrate that short‐term selective costs during selection in one environment can lead to changes in evolvability that confer longer term benefits.     

Complex growth rate evolution in a latitudinally widespread species

The simultaneous effects of selective agents acting on somatic growth rates, their interactions, and their interactions with local environmental conditions that vary across a species' geographic range are potentially complex and poorly known. This is particularly true of viviparous ectotherms whose offspring may be adapted to the gestation environment provided by their mothers. We studied multiple sources of growth rate variation in a widespread, viviparous reptile, including the effect of the maternal environment on growth following parturition. Females in early pregnancy were collected from replicate populations close to the tropical and temperate margins of this species' range. These females completed gestation in either of two different, common environments designed to simulate the thermal and photoperiod environments at the sampling locations. Our experiments revealed complex growth rate evolution between the northern and southern extremes of Eulamprus quoyii's geographic range and local adaptation of growth rates to maternal environments. Unique to this study was the manifestation of these growth rate differences, entrained in utero, but expressed following parturition and maintained through to maturity despite the presence of compensatory growth. In addition to providing the most complete picture to date of the evolution of somatic growth in a viviparous ectotherm, our study suggests that understanding local adaptation to maternal gestation environments, in terms of both mean growth rates and growth rate reaction norms, could change our understanding of how growth rates have evolved in other viviparous ectotherms. Indeed, such local adaptation may provide a selective advantage in the evolution of viviparity.     

Early growth and development of reciprocal hybrids of the starry flounder Platichthys stellatus and stone flounder Kareius bicoloratus

Larval growth and development of hybrid flounder were observed and compared with those of their parent species. The reciprocal hybrids of female starry flounder Platichthys stellatus and male stone flounder Kareius bicoloratus (hybrid Sb) and of female K. bicoloratus and male P. stellatus (hybrid Bs) both survived and grew to juveniles. Development was divided into nine stages (A–I). Many of the hybrids' traits were identical and intermediate to those of their parents. The position of the eye, however, was primarily sinistral in both hybrids (80% in Sb and 76% in Bs), a trait possessed by P. stellatus (80%) in the western Pacific Ocean. The daily growth rates of the larvae were similar. In the parent species, development was more rapid in P. stellatus than in K. bicoloratus whereas rate of development was intermediate in both Sb and Bs hybrids. The size at settlement [standard length (L_S) at stage H (mean ± s.d. )] was 9·82 ± 1·47 mm for the hybrid Sb and 9·99 ± 0·90 mm for the hybrid Bs, while the minimum age at metamorphosis (initial age at stage H) was 29 days after hatching (DAH) in both hybrids. In comparison, L_S at settlement in parent species was 6·43 ± 0·25 mm for P. stellatus and 12·87 ± 1·29 mm for K. bicoloratus. Minimum age at metamorphosis for the parents was 23 DAH at stage G in P. stellatus and 34 DAH at stage H in K. bicoloratus. Thus, the timing of settlement of hybrids was different from that of their parent species. These traits may occur with high frequency in a natural habitat.     

Adaptive evolution to novel predators facilitates the evolution of damselfly species range shifts

Most species have evolved adaptations to reduce the chances of predation. In many cases, adaptations to coexist with one predator generate tradeoffs in the ability to live with other predators. Consequently, the ability to live with one predator may limit the geographic distributions of species, such that adaptive evolution to coexist with novel predators may facilitate range shifts. In a case study with Enallagma damselflies, we used a comparative phylogenetic approach to test the hypothesis that adaptive evolution to live with a novel predator facilitates range size shifts. Our results suggest that the evolution of Enallagma shifting from living in ancestral lakes with fish as top predators, to living in lakes with dragonflies as predators, may have facilitated an increase in their range sizes. This increased range size likely arose because lakes with dragonflies were widespread, but unavailable as a habitat throughout much of the evolutionary history of Enallagma because they were historically maladapted to coexist with dragonfly predators. Additionally, the traits that have evolved as defenses against dragonflies also likely enhanced damselfly dispersal abilities. While many factors underlie the evolutionary history of species ranges, these results suggest a role for the evolution of predator‐prey interactions.     

Adaptive evolution of the insulin gene in caviomorph rodents

Insulin is a conservative molecule among mammals, maintaining both its structure and function. Rodents that belong to the Suborder Hystricognathi represent an exception, having a very divergent molecule with unusual physiological properties. In this work, we analyzed the evolutionary pattern of the insulin gene in caviomorph rodents (South American hystricomorph rodents). We found that these rodents have higher rates of nonsynonymous:synonymous substitutions (d(N)/d(S)) than nonhystricomorph rodents and that values are heterogeneous inside the group. We estimated codons under positive selection, specifically the second binding site (A13 and B17) and others related with hexamerization (B18, B20, and B22). In the monomer structure, all selected sites formed a single patch around the second binding site. In the hexamer structure, these amino acids were grouped into three major patches. In this structure, contacts between B chains involved all selected sites (except B18), and between faces in the center of the molecule, all contacts were among selected sites. While there is no clear hypothesis regarding the cause of this drastic change, experimental evidence does show that this group of rodents has some peculiarities in growth function, and, whether coincidental or not, these changes appeared together with important changes in life-history traits.     

Molecular analysis of heterochronic changes in the evolution of direct developing sea urchins

The sea urchin Heliocidaris erythrogramma is a direct developer; it progresses directly from the gastrula to the juvenile adult without forming a pluteus larva. No larval skeleton is formed by mesenchyme cells, but formation of the juvenile skeleton is accelerated. We have examined two alterations in mesenchyme cell behavior that accompany this striking change in developmental pattern. 1) Rapid cell proliferation produces 1700–2200 mesenchyme cells by mid-gastrula, compared to 30–60 primary mesenchyme cells in species with typical larval development. This change may reflect the accelerated production of adult structures in H. erythrogramma. 2) B2C2 is a monoclonal antibody that recognizes primary (Anstrom et al., 1987) and adult mesenchyme cells associated with skeleton formation in typical developers. The altered pattern of B2C2 staining in H. erythrogramma (e.g., a later initial appearance of the B2C2 antigen) suggests that H. erythrogramma has deleted part of a larval program of development and accelerated its adult program of development. These results indicate that cellular and molecular heterochronies accompany the morphological changes in H. erythrogramma development.     

The evolution of cooperation by the Hankshaw effect

The evolution of cooperation—costly behavior that benefits others—faces one clear obstacle. Namely, cooperators are always at a competitive disadvantage relative to defectors, individuals that reap the benefits, but evade the cost of cooperation. One solution to this problem involves genetic hitchhiking, where the allele encoding cooperation becomes linked to a beneficial mutation, allowing cooperation to rise in abundance. Here, we explore hitchhiking in the context of adaptation to a stressful environment by cooperators and defectors with spatially limited dispersal. Under such conditions, clustered cooperators reach higher local densities, thereby experiencing more mutational opportunities than defectors. Thus, the allele encoding cooperation has a greater probability of hitchhiking with alleles conferring stress adaptation. We label this probabilistic enhancement the “Hankshaw effect” after the character Sissy Hankshaw, whose anomalously large thumbs made her a singularly effective hitchhiker. Using an agent‐based model, we reveal a broad set of conditions that allow the evolution of cooperation through this effect. Additionally, we show that spite, a costly behavior that harms others, can evolve by the Hankshaw effect. While in an unchanging environment these costly social behaviors have transient success, in a dynamic environment, cooperation and spite can persist indefinitely.     

Rates of projected climate change dramatically exceed past rates of climatic niche evolution among vertebrate species

A key question in predicting responses to anthropogenic climate change is: how quickly can species adapt to different climatic conditions? Here, we take a phylogenetic approach to this question. We use 17 time‐calibrated phylogenies representing the major tetrapod clades (amphibians, birds, crocodilians, mammals, squamates, turtles) and climatic data from distributions of > 500 extant species. We estimate rates of change based on differences in climatic variables between sister species and estimated times of their splitting. We compare these rates to predicted rates of climate change from 2000 to 2100. Our results are striking: matching projected changes for 2100 would require rates of niche evolution that are > 10 000 times faster than rates typically observed among species, for most variables and clades. Despite many caveats, our results suggest that adaptation to projected changes in the next 100 years would require rates that are largely unprecedented based on observed rates among vertebrate species.     

The effects of temperature and food on naupliar development,growth and metamorphosis in three species of Boeckella (Copepoda:Calanoida)

Three species of Boeckella (B. triarticulata, B. dilatata and B. hamata) were reared from hatching to copepodite I (CI) at three naturally fluctuating food levels and three temperatures in a 3 × 3 × 3 factorial design. Development times, lengths and mortality were measured for each species in nine treatments. Temperature had the major effect on development times but food level had the major effect on CI lengths. Mortality varied interspecifically with treatment. The combined effect of temperature and food on development times and lengths was species-specific. There were trade-offs between development time and growth to meet constraints imposed by naupliar metamorphosis. The three species varied in the timing of metamorphosis to CI. B. triarticulata nauplii were age determined, B. dilatata nauplii were size determined and B. hamata nauplii were flexibly age and size determined depending on treatment. Differences in life history parameters and the timing of naupliar metamorphosis are discussed in relation to the distributions of the species in ponds (B. triarticulata), glacial lakes (B. dilatata) and coastal lakes (B. hamata) in the South Island of New Zealand.     

Fine structure and development of Triaenophorus nodulosus (Cestoda) during metamorphosis: a review

The results of long‐term investigations of tissue differentiation during metamorphosis in the pseudophyllidean cestode Triaenophorus nodulosus are discussed. The process of tissue reorganization during transformation of the free‐swimming coracidium of T. nodulosus to a parasitic procercoid are studied and the development of all specialized systems (tegumental, muscular, excretory, nervous and glandular) are described and compared. As a consequence, the general cytological mechanism of differentiation has been identified in T. nodulosus. The cytodifferentiation processes are characterized by autophagy of the initial specialized cell population and its replacement by a second population with other morphological and functional potentials. The change in specialized cell populations during morphogenesis is caused by a change in the functional requirements of organs. The primitive nature of the differentiation processes in T. nodulosus at the initial stages of tissue formation is confirmed. It is supposed that destruction of the primary cell populations is the result of apoptosis or genetically programmed suicide.