Heterochrony in plant evolutionary studies through the twentieth century

The evolution of plant morphology is the result of changes in developmental processes. Heterochrony, the evolutionary change in developmental rate or timing, is a major cause of ontogenetic modification during evolution. It is responsible for both interspecific and intraspecific morphological differences. Other causes include heterotopy, the change of structural position, and homeosis, the replacement of a structure by another. This paper discusses and reviews the role of heterochrony in plant evolution at the organismal, organ, tissue, cellular, and molecular levels, as well as the relationships among heterochrony, heterotopy, and homeosis. An attempt has been made to include all published studies through late 1999. It is likely that most heterochronic change involves more than one of the six classic pure heterochronic processes. Of these processes, we found neoteny (decreased developmental rate in descendant), progenesis (earlier offset), and acceleration (increased rate) to be more commonly reported than hypermorphosis (delayed offset) or predisplacement (earlier onset). We found no reports of postdisplacement (delayed onset). Therefore, although rate changes are common (both neoteny and acceleration), shifts in timing most commonly involve earlier termination in the descendant (progenesis). These relative frequencies may change as more kinds of structures are analyzed. Phenotypic effects of evolutionary changes in onset or offset timing can be exaggerated, suppressed, or reversed by changes in rate. Because not all developmental changes responsible for evolution result from heterochrony, however, we propose that plant evolution be studied from a viewpoint that integrates these different developmental mechanisms.     

Heterochrony: Developmental mechanisms and evolutionary results

The concept of heterochrony, that the relative timing of ontogenetic events can shift during evolution, has been a major paradigm for understanding the role of developmental processes in evolution. In this paper we consider heterochrony from the perspective of developmental biology. Our objective is to redefine heterochrony more broadly so that the concept becomes readily applicable to the evolution of the full range of ontogenetic processes, from embryogenesis through the adult. Throughout, we stress the importance of considering heterochrony from a hierarchical perspective. Thus, we recognize that a heterochronic change at one level of organization may be the result of non-heterochronic events at an underlying level. As such, heterochrony must be studied using a combination of genetic, molecular, cellular, and morphological approaches.     

Nonheterochronic developmental changes underlie morphological heterochrony in the evolution of the Ardeidae

Evolutionary changes in developmental timing and rates (heterochrony) are a source of morphological variation. Here we explore a central issue in heterochronic analysis: are the alterations in developmental timing and rates the only factor underlying morphological heterochrony? Tarsometatarsal growth through endochondral ossification in Ardeidae evolution has been taken as a case study. Evolutionary changes in bone growth rate (morphological heterochrony) might be either (a) the result of alterations in the mitotic frequency of epiphyseal chondrocytes (process‐heterochrony hypothesis), or (b) the outcome of alterations in the number of proliferating cells or in the size of hypertrophic chondrocytes (structural hypothesis). No correlation was found between tarsometatarsal growth rates and the frequency of cell division. However, bone growth rates were significantly correlated with the number of proliferating cells. These results support the structural hypothesis: morphological acceleration and deceleration are the outcome of evolutionary changes in one structural variable, the number of proliferating cells.     

The nuclear receptor gene nhr-25 plays multiple roles in the Caenorhabditis elegans heterochronic gene network to control the larva-to-adult transition

Developmental timing in the nematode Caenorhabditis elegans is controlled by heterochronic genes, mutations in which cause changes in the relative timing of developmental events. One of the heterochronic genes, let-7, encodes a microRNA that is highly evolutionarily conserved, suggesting that similar genetic pathways control developmental timing across phyla. Here we report that the nuclear receptor nhr-25, which belongs to the evolutionarily conserved fushi tarazu-factor 1/nuclear receptor NR5A subfamily, interacts with heterochronic genes that regulate the larva-to-adult transition in C. elegans. We identified nhr-25 as a regulator of apl-1, a homolog of the Alzheimer's amyloid precursor protein-like gene that is downstream of let-7 family microRNAs. NHR-25 controls not only apl-1 expression but also regulates developmental progression in the larva-to-adult transition. NHR-25 negatively regulates the expression of the adult-specific collagen gene col-19 in lateral epidermal seam cells. In contrast, NHR-25 positively regulates the larva-to-adult transition for other timed events in seam cells, such as cell fusion, cell division and alae formation. The genetic relationships between nhr-25 and other heterochronic genes are strikingly varied among several adult developmental events. We propose that nhr-25 has multiple roles in both promoting and inhibiting the C. elegans heterochronic gene pathway controlling adult differentiation programs.     

A genetic basis for intraspecific differences in developmental timing?

Heterochrony, altered developmental timing between ancestors and their descendents, has been proposed as a pervasive evolutionary feature and recent analytical approaches have confirmed its existence as an evolutionary pattern. Yet, the mechanistic basis for heterochrony remains unclear and, in particular, whether intraspecific variation in the timing of developmental events generates, or has the potential to generate, future between‐species differences. Here we make a key step in linking heterochrony at the inter‐ and intraspecific level by reporting an association between interindividual variation in both the absolute and relative timing (position within the sequence of developmental events) of key embryonic developmental events and genetic distance for the pond snail, Radix balthica. We report significant differences in the genetic distance of individuals exhibiting different levels of dissimilarity in their absolute and relative timing of developmental events such as spinning activity, eyespot formation, heart ontogeny, and hatching. This relationship between genetic and developmental dissimilarity is consistent with there being a genetic basis for variation in developmental timing and so suggests that intraspecific heterochrony could provide the raw material for natural selection to produce speciation.     

The role of time and timing in hominid dental evolution

Exactly when during evolution hominids acquired their extended extra-uterine growth period is a contentious issue. In order to shed light on the tempo and mode of ontogenetic changes during hominid evolution, research has focused on the pattern and, to a lesser extent, the rate of growth observed in the developing dentition of extant and extinct hominoid taxa. From these data, the absolute timing of events has often been inferred, either implicitly or explicitly. Differences in patterns of growth, especially of the eruption of teeth, are reasonably well documented among hominoids. However, data on the absolute timing of dental developmental events are much more scarce, rendering tentative all inferences about timing from patterns alone. Such inferences are even more tentative when they involve interpreting ontogenetic trajectories in extinct species such as Plio-Pleistocene hominids, which almost certainly had unique patterns of maturation. In order to contribute to the debate about possible relations between pattern and timing in the developing dentition, we have collated information that specifically relates to the absolute timing of developmental events in extant and extinct hominoids and, hence, also to the rate at which processes occur. In doing so, we have attempted to identify both developmental constraints and possible heterochronic processes that may have led to the extended growth period characteristic of humans. There appears to be growing evidence that evolution toward an extended hominid ontogeny did not follow a path that can be described as a simple heterochronic event.     

Morphological evolution in Ceratophryinae frogs (Anura,Neobatrachia): the effects of heterochronic changes during larval development and metamorphosis

Heterochrony produces morphological change with effects in shape, size, and/or timing of developmental events of a trait related to an ancestral ontogeny. This paper analyzes heterochrony during the ontogeny of Ceratophryinae (Ceratophrys, Chacophrys, and Lepidobatrachus), a monophyletic group of South American frogs with larval development, and uses different approaches to explore their morphological evolution: (1) inferences of ancestral ontogenies and heterochronic variation from a cladistic analysis based on 102 morphological larval and adult characters recorded in ten anuran taxa; (2) comparisons of size, morphological variation, and timing (age) of developmental events based on a study of ontogenetic series of ceratophryines, Telmatobius atacamensis, and Pseudis platensis. We found Chacophrys as the basal taxon. Ceratophrys and Lepidobatrachus share most derived larval features resulting from heterochrony. Ceratophryines share high rates of larval development, but differ in rates of postmetamorphic growth. The ontogeny of Lepidobatrachus exhibits peramorphic traits produced by the early onset of metamorphic transformations that are integrated in an unusual larval morphology. This study represents an integrative examination of shape, size, and age variation, and discusses evolutionary patterns of metamorphosis. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154 , 752–780.     

THE HETEROCHRONIC ORIGIN OF THE CLEISTOGAMOUS FLOWER IN ASTRAGALUS CYMBICARPOS (FABACEAE)

Members of the species Astragalus cymbicarpos form chasmogamous and cleistogamous flowers, as well as a large variety of intermediate floral types. Bivariate allometry and Gould's clock models were used to investigate the possible heterochronic evolution of the cleistogamous flower from the chasmogamous flower. In three of the whorls analyzed (pistil, stamens, and corolla) comparison of chasmogamous, pseudocleistogamous, and cleistogamous flowers revealed a progressive “juvenilization” of the adult form. This paedomorphic morphology proved to be partly the result of a process of progenesis, also evident in acceleration of sexual maturity. The retardation of shape with respect to size in these three whorls suggests, however, the existence of a heterochronic process other than progenesis.     

Heterochronic shifts explain variations in a sequentially developing repeated pattern: palatal ridges of muroid rodents

SUMMARY Metazoans are largely made of repeated parts, and metazoan evolution is marked by changes in the number of these parts, called meristic evolution. Understanding the mechanisms associated with meristic changes is thus a critical issue to evolutionary developmental biology. Palatal rugae are sensory ridges regularly arranged on the hard palate of mammals. They develop sequentially following mesio-distal growth of the palate, and activation–inhibition mechanisms very likely control spacing and timing of this sequential addition. In this study, we characterized trends in rugae number evolution among muroid rodents, showing that most species display 8±1 rugae, changes by one being very frequent in the phylogeny. We then compared development of three muroid species: mouse (nine rugae), rat (eight), and golden hamster (seven). We showed that palatal growth rate, spacing, and addition rate in mouse/rat were remarkably similar (with respect to the embryo size difference), and that increase to nine rugae in mouse is achieved by postponing the end of the addition process (hypermorphosis). Such a heterochronic shift may be typical of ±1 variations observed among muroid rodents. In contrast, decrease to seven rugae in golden hamster is attributed to early growth termination (progenesis) of the palate, which correlates with the severe shortening of gestation in this species. Our results provide an experimental support to the intuitive view that heterochronies are especially relevant to meristic evolution of traits that rely on a sequential addition process. We also interpret our results in the light of developmental constraints specifically linked to this kind of process.     

Parent–offspring similarity in the timing of developmental events: an origin of heterochrony?

Understanding the link between ontogeny (development) and phylogeny (evolution) remains a key aim of biology. Heterochrony, the altered timing of developmental events between ancestors and descendants, could be such a link although the processes responsible for producing heterochrony, widely viewed as an interspecific phenomenon, are still unclear. However, intraspecific variation in developmental event timing, if heritable, could provide the raw material from which heterochronies originate. To date, however, heritable developmental event timing has not been demonstrated, although recent work did suggest a genetic basis for intraspecific differences in event timing in the embryonic development of the pond snail, Radix balthica. Consequently, here we used high-resolution (temporal and spatial) imaging of the entire embryonic development of R. balthica to perform a parent–offspring comparison of the timing of twelve, physiological and morphological developmental events. Between-parent differences in the timing of all events were good predictors of such timing differences between their offspring, and heritability was demonstrated for two of these events (foot attachment and crawling). Such heritable intraspecific variation in developmental event timing could be the raw material for speciation events, providing a fundamental link between ontogeny and phylogeny, via heterochrony.     

Variance in developmental event timing is greatest at low biological levels: implications for heterochrony

Intraspecific variation in developmental event timing is common and may be the raw material from which heterochronies (altered timing of developmental events between ancestors and descendants) arise. However, our understanding of how variance in intraspecific developmental event timing is distributed across different hierarchical, biological levels is poor, despite recent evidence suggesting a genetic basis for such inter‐individual differences. In the present study, we used high (temporal and spatial) resolution bio‐imaging of the entire embryonic development of the pond snail, Radix balthica, to investigate how variance was partitioned between the biological levels of interpopulation, inter‐egg mass and individual, with respect to the relative timing of four key developmental events (four‐cell division, a discrete heart beat, capsule rupture, and hatching), as well as egg volume (an index of maternal investment), hatchling size and shape (to compare embryonic with post‐hatch variance). We found that the timing of all but one (four cell division) of the developmental events, together with all measures of hatchling size and shape, had most variance partitioned at the individual level; variance at the interpopulation level was surprisingly low despite sampling populations from across the geographical range of R. balthica. These patterns highlight the importance of studying the distribution of variance in developmental event timing with the aim of understanding how it might drive organismal ecology and evolution. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 581–590.     

Activation of nicotinic receptors uncouples a developmental timer from the molting timer in C. elegans

C. elegans develops through four larval stages (L1 to L4) separated by molts. The identity of larval stages is mostly determined by stage-specific expression of heterochronic genes, which constitute an intrinsic genetic timer. However, extrinsic cues such as food availability or population density also modulate the developmental timing of C. elegans by mechanisms that remain largely unknown. To investigate a potential role of the nervous system in the temporal regulation of C. elegans development, we pharmacologically manipulated nicotinic neurotransmission, which represents a prominent signaling component in C. elegans nervous system. Exposure to the nicotinic agonist DMPP during post-embryonic development is lethal at the L2/L3 molt. Specifically, it delays cell divisions and differentiation during the L2 stage but does not affect the timing of the molt cycle, hence causing exposure of a defective L3 cuticle to the environment after the L2/L3 molt. Forcing development through a previously uncharacterized L2 diapause resynchronizes these events and suppresses DMPP-induced lethality. Nicotinic acetylcholine receptors (nAChRs) containing the UNC-63 subunit are required, probably in neurons, to trigger the action of DMPP. Using a forward genetic screen, we further demonstrated that the nuclear hormone receptor (NHR) DAF-12 is necessary to implement the developmental effects of DMPP. Therefore, a novel neuroendocrine pathway involving nAChRs and the NHR DAF-12 can control the speed of stage-specific developmental events in C. elegans. Activation of DMPP-sensitive nAChRs during the second larval stage uncouples a molting timer and a developmental timer, thus causing a heterochronic phenotype that is lethal at the subsequent molt.     

Morphological and growth rate differences among outcrossing and self-pollinating races of Arenaria uniflora (Caryophyllaceae)

Populations of Arenaria uniflora exhibit intraspecific variation in floral size and degree of protandry in association with the evolution of self-pollination. Heterochrony, or a simple change in the absolute timing or rate of developmental events, is proposed as the evolutionary mechanism underlying the origin of the small, self-pollinating flowers from their large, outcrossing progenitors. Inflorescence growth in two autogamous populations and their related outcrossing progenitors was studied to provide the temporal data necessary for testing the hypothesis of heterochrony. All four races showed significant variation in the growth and mature length of inflorescence organs. Inflorescences of selfing races were smaller, and had slower relative growth rates and a two-fold increase in the plastochron relative to outcrossing populations. The large-flowered races were both significantly protandrous. A more detailed growth analysis of flower development in two races indicated that the selfing flowers develop at a slower rate and for a longer duration relative to outcrossing flowers. The implications of these temporal changes in floral ontogeny for the heterochronic origin of self-pollinating floral forms are considered.     

Cleistogamous capitulum in Centaurea melitensis (Asteraceae): heterochronic origin

Cleistogamous capitula formed by Centaurea melitensis display a number of morphological and functional changes with respect to chasmogamous capitula that ensure self-fertilization. Because no studies have hitherto addressed the evolution of cleistogamy in Asteraceae, it was considered useful to ascertain whether these changes are attributable to one or more of the heterochronic processes reported in the literature. Bivariate allometric analyses were performed, and changes were represented graphically using Gould's clock models for size, shape, and age of several capitulum and floret structures. Results suggest that the partially paedomorphic appearance of cleistogamous with respect to chasmogamous capitula is attributable to three processes: (1) early onset of floral development (predisplacement), (2) decreased growth rate of the whorls studied (except gynoecium width) and (3) early offset time (progenesis). The latter appears to play the most significant role in the origin of the cleistogamous capitulum.     

The molecular evolution of development

Morphological differences between species, from simple single-character differences to large-scale variation in body plans, can be traced to changes in the timing and location of developmental events. This has led to a growing interest in understanding the genetic basis behind the evolution of developmental systems. Molecular evolutionary genetics provides one of several approaches to dissecting the evolution of developmental systems, by allowing us to reconstruct the history of developmental genetic pathways, infer the origin and diversification of developmental gene functions, and assess the relative contributions of various evolutionary forces in shaping regulatory gene evolution. BioEssays 20 :700–711, 1998. © 1998 John Wiley & Sons, Inc.     

Can heterochrony help explain the high morphological diversity within the genus Niphargus (Crustacea: Amphipoda)?

Postembryonic development of nine species of Niphargus (Crustacea: Amphipoda) was studied, with spine development and shifts in allometric growth being combined in developmental sequences that were compared across species. The developmental sequences show high diversity with respect to the position of individual events in the sequence, as well as a high frequency of events being inapplicable in some species. Within Niphargus, the highest degree of independence between events occurs mainly in early mid-aged instars, where the shifts in position are both the largest in magnitude and also the most frequent in occurrence. Constructive troglomorphic features of subterranean species were inferred to develop more because of accelerated growth rather than a delayed offset of growth. Shifts in both relative timing and growth rate appeared to have played a role in the evolution of sexually dimorphic elongated appendages. Growth patterns differed greatly between species for individual sexually dimorphic and troglomorphic traits, hinting at their possible independent origin. The independence between developmental events that was generally apparent might indicate the existence of an important genetic basis for the extreme intrageneric morphological variation arising from numerous highly variable body parts being combined in a ‘mosaic’ manner. Moreover, we suggest that the overall diversity of the genus might actually be underestimated in light of possible convergent features accompanied by ‘cryptic’ speciation. We conclude that both sequential and growth heterochrony appear to have played a key role in the evolution of Niphargus, the most diverse genus of freshwater amphipods. A preliminary list of heterochronic characters is provided.     

PASOS: a method for the phylogenetic analysis of shape ontogenies

We present a novel phylogenetic approach to infer ancestral ontogenies of shape characters described as landmark configurations. The method is rooted in previously published theoretical developments to analyse landmark data in a phylogenetic context with parsimony as the optimality criterion, in this case using the minimization of differences in landmark position to define not only ancestral shapes but also the changes in developmental timing between ancestor–descendant shape ontogenies. Evolutionary changes along the tree represent changes in relative developmental timing between ontogenetic trajectories (possible heterochronic events) and changes in shape within each stage. The method requires the user to determine the shape of the specimens between two standard events, for instance birth and onset of sexual maturity. Once the ontogenetic trajectory is discretized into a series of consecutive stages, the method enables the user to identify changes in developmental timing associated with changes in the offset and/or onset of the shape ontogenetic trajectories. The method is implemented in a C language program called SPASOS. The analysis of two empirical examples (anurans and felids) using this novel method yielded results in agreement with previous hypotheses about shape evolution in these groups based on non-phylogenetic analyses.