Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships

Evolutionary developmental biology ("evo-devo") has revolutionized evolutionary biology but has had relatively little impact on systematics. We show that similar large-scale developmental changes in distantly related lineages can dramatically mislead phylogenetic analyses based on morphological data. Salamanders are important model systems in many fields of biology and are of special interest in that many species are paedomorphic and thus never complete metamorphosis. A recent study of higher-level salamander phylogeny placed most paedomorphic families in a single clade based on morphological data. Here, we use new molecular and morphological data to show that this result most likely was caused by the misleading effects of paedomorphosis. We also provide a well-supported estimate of higher-level salamander relationships based on combined molecular and morphological data. Many authors have suggested that paedomorphosis may be problematic in studies of salamander phylogeny, but this hypothesis has never been tested with a rigorous phylogenetic analysis. We find that the misleading effects of paedomorphosis on phylogenetic analysis go beyond the sharing of homoplastic larval traits by paedomorphic adults, and the problem therefore is not solved by simply excluding suspected paedomorphic characters. Instead, two additional factors are critically important in causing paedomorphic species to be phylogenetically "misplaced": (1) the absence of clade-specific synapomorphies that develop during metamorphosis in nonpaedomorphic taxa and allow their "correct" placement and (2) parallel adaptive changes associated with the aquatic habitat of the larval stage. Our results suggest that the effects of paedomorphosis on phylogenetic analyses may be complex, difficult to detect, and can lead to results that are both wrong and statistically well supported by parsimony and Bayesian analyses.     

A rhinesuchid-like temnospondyl from the Permo-Triassic of Uruguay

A new temnospondyl species, Arachana nigra, from the Permo-Triassic Buena Vista Formation of Uruguay is described. The holotypic and only known specimen consists of an almost complete skull lacking most of the snout, the tabular horns and the posterolateral corners of the skull table. As with other specimens from the same unit, Arachana shows a transitional morphology. It shares several characters with rhinesuchids, such as the large size and the general shape of the skull, orbits positioned slightly posterior to the skull roof mid-length, a coarsely pitted dermal ornamentation lacking pustules, and a smoothly convex cheek contour. The palatal ramus of the pterygoid suturing with the vomer, and excluding the palatine and ectopterygoid from the margin of the interpterygoid vacuity, and the presence of a small basioccipital, visible in both occipital and ventral view, also resemble the conditions found in rhinesuchids and other basal temnospondyls. Other characters present in Arachana, however, are commonly found in lydekkerinids, but are absent in almost all rhinesuchids: supratemporal excluded from otic notch; supraorbital and infraorbital sensory sulci encroaching the lacrimal, although lacking a step-like lacrimal flexure; otic notch not deeply incised; post-temporal fenestra large and rounded; occipital condyles well-separated from each other; palatine tooth row behind the palatine tusk reduced; pterygoid corpus slightly ornamented; and presence of an interorbital depression. This combination of primitive and derived characters is consistently present in most components of the Buena Vista fauna, which could thus be transitional between typical Permian and Triassic tetrapod communities found elsewhere. The location of the PTB in the Uruguayan sequence is controversial, mainly due to the lack of clear faunal correlations with other well-known sequences, such as those of southern Africa and Russia. Moreover, the mosaic-like character combinations in most of the recorded tetrapods ally them to both Triassic and Paleozoic groups, and this has complicated even more the possibility of age assignment. Transitional faunas associated with the PTB, such as the Russian Uppermost Permian faunas, could be equivalent to the unique Colonia Orozco fauna. If true, this scenario will substantially change estimates about survivorship rates, suggesting a speciation rate increase in temnospondyls after the Permian-Triassic event. Based on taxonomic, phylogenetic, and geochronologic data, the Buena Vista fauna allows us to quantify faunal turnover across the PTB and in the aftermath of the end Permian extinction event.     

The genus Teliocrinus (Crinoidea,Echinodermata): a key taxon among pentacrinid stalked crinoids

The main characters of the stalked crinoids of the family Pentacrinitidae attributed to the genus Teliocrinus are re‐evaluated from a quantitative study of phenotype variation, new observations on arm and stalk articulations, and observation of ontogenetic trends. All of the specimens collected in the northern Indian Ocean belong to the same species, i.e. Teliocrinus springeri (Clark, 1909). However, two phenotypes living at different depths remain valid as subspecies: Teliocrinus springeri springeri (Clark, 1909) and Teliocrinus springeri liliaceus (Clark, 1909). Teliocrinus shares several ontogenetic trends with Endoxocrinus, especially in nonfunctional brachial articulations and stalk symplexies. Its assignment to the Diplocrininae is confirmed. A discussion of its affinities with pentacrinid fossil genera in which the crown is well preserved suggests that Diplocrininae could have first appeared during the Lower Cretaceous. A shortening of brachitaxes and a paedomorphic trend of stalk symplexies are the main other evolutionary traits. Nonfunctional articulations are frequently found at the paedomorphic pole of the heterochronic gradient, without clear derived characters. Classification of pentacrinids mainly based on such symplesiomorphy or paedomorphic characters must be definitively abandoned. However, in post‐Palaeozoic stalked crinoids the scarcity of well‐preserved fossils, the high frequency of paedomorphy, and convergent adaptive characters makes phylogenetic reconstruction only based on morphological characters very difficult and speculative. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155 , 22–39.     

Geometric shell growth and mode of life of a Devonian chonetoidean brachiopod

Morphological and statistical analysis of the chonetoid species Kentronetes variabilis from the Lower Devonian (Lochkovian) of the Argentine Precordillera demonstrate ontogenetic changes and allometric relationships between characters. A special study was made of spine distribution, morphology, and growth, compared to valve growth. The first, inner, developed spines (pairs 1–1'and 2–2') continued to grow after development of the following outer pairs. The spacing of spines, their diameter, and the density of growth rings vary from beak to posterolateral margins following a specific 2ⁿ geometric growth factor, compared to the regular, almost linear growth of the valves, attested by growth lines. The linear growth rate of outer spines (pairs 3–3'and 4–4') can be 6–8 times more rapid than that of the shell on the valve margin. Ontogenetic changes in spine morphology are interpreted as a response to changes in the mode of life.     

Paedomorphosis as an Evolutionary Driving Force: Insights from Deep-Sea Brittle Stars

Heterochronic development has been proposed to have played an important role in the evolution of echinoderms. In the class Ophiuroidea, paedomorphosis (retention of juvenile characters into adulthood) has been documented in the families Ophiuridae and Ophiolepididae but not been investigated on a broader taxonomic scale. Historical errors, confusing juvenile stages with paedomorphic species, show the difficulties in correctly identifying the effects of heterochrony on development and evolution. This study presents a detailed analysis of 40 species with morphologies showing various degrees of juvenile appearance in late ontogeny. They are compared to a range of early ontogenetic stages from paedomorphic and non-paedomorphic species. Both quantitative and qualitative measurements are taken and analysed. The results suggest that strongly paedomorphic species are usually larger than other species at comparable developmental stage. The findings support recent notions of polyphyletic origin of the families Ophiuridae and Ophiolepididae. The importance of paedomorphosis and its correct recognition for the practice of taxonomy and phylogeny are emphasized.     

Reinterpreting recapitulation: systematics of needlefishes and their allies (Teleostei: Beloniformes)

Abstract. As needlefishes (Belonidae) grow, their jaws pass through a "halfbeak" stage that resembles the adult jaw condition of the closely related family of halfbeaks (Hemiramphidae). Based on this pattern, some authors have suggested that halfbeaks are "developmentally arrested" or paedomorphic needlefish derivatives, whereas others have supported the notion that needlefishes are descended from halfbeak-like ancestors and that needlefish ontogeny thereby recapitulates phylogeny. To test these ideas and to better understand evolutionary changes in jaw ontogeny, phylogenetic relationships among genera of needlefishes, sauries (Scomberesocidae), halfbeaks, and flyingfishes (Exocoetidae) were assessed using mitochondrial (cytochrome b and 16S), nuclear (Tmo-4C4), and morphological characters. The resultant tree provides several novel taxonomic findings: (1) flyingfishes appear to be nested within halfbeaks; (2) sauries appear to be nested within needlefishes; and (3) the Indo-West Pacific freshwater halfbeaks appear to be most closely related to the needlefish/saury clade. The structure of the tree falsifies the idea that halfbeaks are paedomorphic needlefishes. Instead, halfbeaks are basal relative to needlefishes, fitting the pattern predicted by the hypothesis of recapitulation. I discuss limitations to phylogenetic perspectives on recapitulation based on discrete character data by comparing aspects of von Baerian and Haeckelian views of the relation between ontogeny and phylogeny.     

The phylogenetic position of an undescribed paedomorphic clupeiform taxon: mitogenomic evidence

Molecular characters may offer a useful alternative to confidently estimate the phylogenetic position of paedomorphic taxa otherwise difficult to place based on morphology because of the reduction or absence of characters in their larvae-like adult stage. Here, we sequenced the complete mitogenome of a remarkable undescribed marine paedomorphic clupeiform fish to gain insight into its phylogenetic position. Of a length of 17,507 bp, this mitogenome exhibits a unique gene order within the Teleostei because of the inversion of the contiguous tRNA^Gln and tRNA^Ile within the IQM region and the presence of a putative second control region inserted between these tRNAs. Mitogenomic data from 27 clupeiform species and 22 non-clupeiform species were subjected to partitioned maximum likelihood and Bayesian analyses. All resultant phylogenetic trees strongly supported the placement of this undescribed taxon within the order Clupeiformes, suborder Clupeoidei, and the family Clupeidae, as the sister group of the tribe Spratelloidini (Jenkinsia + Spratelloides) of the subfamily Dussumieriinae. Together, they form a monophyletic group with Chirocentrus and, possibly, Etrumeus. Despite its overall resemblance to Sundasalanx, this undescribed taxa (Clupeidae gen. et sp. indet.) is not closely related to that genus and represents an independent paedomorphic lineage within the Clupeoidei. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

A Paedomorphic Origin of the Oligomerous Animals?

Anatomical, developmental, and functional studies have demonstrated that the protostone Phoronida (Tentaculata/Lophophorata) share several characters in common with more primitive deuterostomes, thus belonging to the Oligomera and suggesting a level of direct connection between higher (coelomate) Gastroneuralia and lower Deuterostomia. In reevaluation of the characters of the cleavage, the tentacle apparatus, the mesoderm-coelom organization, the nervous system, and also the fate of the blastopore, there is essential support for an evolutionary differentiation of bilaterian animals along a monolinear sequence of recent megagroups (in contrast to other theories): As still reflected by the Phoronida, such monolinear pathway from mesenchymatous to coelomate Gastroneuralia (Spiralia) to Heteroneuralia (Oligomera) to Notoneuralia (Chordata) was made possible predominantly by decisive paedomorphic processes for the tentacles and the nervous system in gastroneuralian pre-Heteroneuralia.     

Parallelisms in the evolution of sea cucumbers (Echinodermata: Holothuroidea)

The importance of taking into account parallelisms in the evolution of morphological characters is analyzed for the taxonomy of the class Holothuroidea. The establishment of the order Dactylochirotida and classification of the order Elasipodida serve as examples to illustrate insufficient appreciation of parallelisms in Holothuroidea. The following characters, evolving independently in different groups of sea cucumbers, are considered: a stout skeleton, reduction of the calcareous ring and the body wall sclerites; similarity of body shape; similarity in the shape of tentacles; reduction in the number of tentacles from 12 to 10 in different fam-ilies and subfamilies of the order Synaptida. Based on the analysis of morphological and molecular data, the family Deimatidae is transferred from the order Elasipodida to the order Aspidochirotida. It is hypothesized that the concave cup-shaped sclerites with three to five rays occurring in the family Laetmogonidae (order Elasipodida) are of paedomorphic origin and correspond to the early growth stages of the laetmogonid wheels; the concave cross-shaped sclerites of the families Elpidiidae and Psychropotidae may have originated from laetmogonid concave cup-shaped sclerites. Emended diagnosis of the order Elasipodida is proposed. The family Vaneyellidae previously synonymized by the author with the family Cucumariidae is reestablished, and its emended diagnosis is also proposed.     

Xylem heterochrony: an unappreciated key to angiosperm origin and diversifications

All angiosperms can be arranged along a spectrum from a preponderance of juvenile traits (cambial activity lost) to one of nearly all adult characters (cambium maximally active, mature patterns realized rapidly early in ontogeny). Angiosperms are unique among seed plants in the width of this spectrum. Xylem patterns are considered here to be indicative of contemporary function, not relictual. Nevertheless, most families of early‐divergent angiosperms exhibit paedomorphic xylem structure, a circumstance that is most plausibly explained by the concept that early angiosperms had sympodial growth forms featuring limited accumulation of secondary xylem. Sympodial habits have been retained in various ways not only in early‐divergent angiosperms, but also among eudicots in Ranunculales. The early angiosperm vessel, relatively marginal in conductive abilities, was improved in various ways, with concurrent redesign of parenchyma and fibre systems to enhance conductive, storage and mechanical capabilities. Flexibility in degree of cambial activity and kinds of juvenile/adult expressions has been basic to diversification in eudicots as a whole. Sympodial growth that lacks cambium, such as in monocots, provides advantages by various features, such as organographic compartmentalization of tracheid and vessel types. Woody monopodial eudicots were able to diversify as a result of production of new solutions to embolism prevention and conductive efficiency, particularly in vessel design, but also in parenchyma histology. Criteria for paedomorphosis in wood include slow decrease in length of fusiform cambial initials, predominance of procumbent ray cells and lesser degrees of cambial activity. Retention of ancestral features in primary xylem (the ‘refugium’ effect) is, in effect, a sort of inverse evidence of acceleration of adult patterns in later formed xylem. Xylem heterochrony is analysed not only for all key groups of angiosperms (including monocots), but also for different growth forms, such as lianas, annuals, various types of perennials, rosette trees and stem succulents. Xylary phenomena that potentially could be confused with heterochrony are discussed. Heterochronous xylem features seem at least as important as other often cited factors (pollination biology) because various degrees of paedomorphic xylem are found in so many growth forms that relate in xylary terms to ecological sites. Xylem heterochrony can probably be accessed during evolution by relatively simple gene changes in a wide range of angiosperms and thus represents a current as well as a past source of variation upon which diversification was based. Results discussed here are compatible with both current molecular‐based phylogenetic analyses and all recent physiological work on conduction in xylem and thus represent an integration of these fields. © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161 , 26–65.     

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.     

Ontogeny and evolution within the Myophorellidae (Bivalvia): Paedomorphic trends

The role of heterochronic phenomena in molluscan evolution is insufficiently understood but potentially significant. The aim of this paper is to explore some paedomorphic trends in the evolution of the Myophorellidae (Bivalvia: Trigoniida). Early ontogeny of general shell shape and ornamentation of one species of Steinmanella was analyzed and compared to data obtained for three species of Myophorella: two belonging to the subgenus M. (Promyophorella) (one from the Jurassic and one from the Cretaceous) and one belonging to the Jurassic M. (Myophorella). For general shell shape, a geometric morphometric analysis was performed on lateral views of the shells. Regarding ornamentation, flank costal disposition on the marginal carina, tubercle separation and relative development of the sub-commarginal subset of flank costae were quantified. A qualitative analysis was also performed. A two-trend shell shape development is considered as primitive. The first trend is marked by a relative reduction of the posterior margin together with a relative elongation of the shell. A tangential opisthogyrate growth component characterizes the second trend. There is a transitional stage where both trends interact. Early flank ornamentation is characterized by two or three sub-commarginal costae, continuous through the area, after which oblique costae with fine tubercles start to form. The subgenus M. (Myophorella) evolved by paedomorphic retention of juvenile shell shape and ornamentation, resulting in a large shell with coarse tubercles. Shell morphology in Steinmanella evolved by paedomorphic suppression of the primitive second trend in the development of the shell, resulting in an orthogyrate shell shape, and the retention of juvenile ornamentation (coarse tubercles, more sub-commarginal costae, juvenile rates of costal disposition). The paedomorphic (most likely by deceleration) retention of juvenile shell morphology within the Myophorellidae seems to have been recurrent within the group, resulting in many cases of convergence, and obscuring the phylogenetic relationships among its species.     

PHYLOGENETIC INTERRELATIONSHIPS AND REDUCTIVE EVOLUTION IN NEOTROPICAL CHARACIDIIN FISHES (CHARACIFORMES, OSTARIOPHYSI)

Abstract— Miniaturization, which results in the presence of numerous apparently paedomorphic characters associated with reduced size, is a common phenomenon among neotropical fishes, with over 85 miniature species distributed among the five major ordinal groups. Eleven species are recognized as miniatures within the Characidiinae, a monophyletic subunit of Characiformes. A reconstruction of characidiin phylogeny is used to analyze the history of miniaturization events. Former hypotheses of origin of miniaturization among characidiins are rejected, underscoring the need for phylogenetic frameworks in the study of ontogenetic changes associated with the phenomenon of miniaturization. The 11 instances of miniature species can be most parsimoniously attributed to three independent miniaturization events within the Characidiinae.
Reductive characters comprise a large proportion of phylogenetically informative characters within the Characidiinae. In the largest group of miniatures, reductive characters represent more than half of the character state transformations affecting supraspecific relationships among Elachocharax, Klausewitzia, Odontocharacidium and Microcharacidium . An analysis of patterns of character state distributions fails to reject the null hypothesis of character independence. A distinction is made between the concepts of character independence, defined as the origination of character states from different (non-simultaneous) evolutionary events, and character correlation, defined as the association of character states in terminal taxa. Character correlation is not a sufficient criterion to reject Hennig's auxiliary principle, according to which the "presence of apomorphous characters in different species is always reason for suspecting kinship, and their origin by convergence should not be assumed a priori". High values of character correlation are the expected result of congruent patterns of character distribution.     

Evaluating paedomorphic heterochrony in trilobites: the case of the diminutive trilobite Flexicalymene retrorsa minuens from the Cincinnatian Series (Upper Ordovician), Cincinnati region

Flexicalymene retrorsa minuens from the uppermost 3 m of the Waynesville Formation of the Cincinnatian Series (Upper Ordovician) of North America lived approximately 445 Ma and exhibited marked reduction in maximum size relative to its stratigraphically subjacent sister subspecies, Flexicalymene retrorsa retrorsa. Phylogenetic analysis is consistent with the notion that F. retrorsa retrorsa was the ancestor of F. retrorsa minuens. F. retrorsa minuens has been claimed to differ from F. retrorsa retrorsa"in size alone," and thus presents a plausible example of global paedomorphic evolution in trilobites. Despite strong similarity in the overall form of the two subspecies, F. retrorsa minuens is neither a dwarf nor a simple progenetic descendant of F. retrorsa retrorsa. More complex patterns of global heterochronic paedomorphosis, such as a neotonic decrease in the rate of progress along a common ontogenetic trajectory with respect to size, coupled with growth cessation at a small size, "sequential" progenesis, or non-uniform changes in the rate of progress along a shared ontogenetic trajectory with respect to size, can also be rejected. Rather, differences between these subspecies are more consistent with localized changes in rates of character development than with a global heterochronic modification of the ancestral ontogeny. The evolution of F. retrorsa minuens from F. retrorsa retrorsa was largely dominated by modifications of the development of characters already evident in the ancestral ontogeny, not by the origin of novel structures. Factors promoting size reduction in F. retrorsa minuens appear to have been specific to this subspecies, because other co-occurring taxa, including other trilobite species, do not show marked differences in mean size.     

Paedomorphosis of ammonoids as a result of sealevel fluctuations in the Late Devonian Wocklumeria Stufe

A remarkable diversification of several independent ammonoid lineages with high evolutionary rates occurred in the Late Devonian Wocklumeria Stufe. Many speciation events led to paedomorphic ammonoids that display a striking range of conch shapes, sculpture, and ornamentation. In the goniatite family Prionoceratidae, the transition from normal Mimimitoceras species to paedomorphic Balvia species provides an example of rapid size decrease combined with an early character developmental offset arising from progenesis. Adults of early Balvia species largely have the preadult ancestral morphology of Mimimitoceras , but later evolving species acquire distinct conch and ornamentation types. Progenetic ammonoid species also appeared within the clymeniid family Kosmoclymeniidae and probably in the Glatzielliidae. In the clymeniid family Parawocklumeriidae, evolution is characterized by the extension of tri-segmented and triangularly coiled whorls found only in juveniles of earlier species, to the adults of later species. This is interpreted as resulting from neoteny. The distribution of paedomorphic ammonoids in the Late Devonian Wocklumeria Stufe is closely correlated to relative sealevel changes. The regressive trend in the lower two-thirds of the Wocklumeria Stufe is interpreted as the cause of a diversification of the pelagic habitat during unstable conditions, and as an extrinsic factor inducing heterochronic change. Some ammonoids reacted by rapid maturation and faster reproductive rates, giving the opportunity to exploit a wider range of niches. The apparent consequence was the formation of several allopatric species. □ Ammonoidea, Late Devonian, evolution, heterochrony, sealevel changes.     

CRANIAL MORPHOLOGY OF DOMESTIC AND WILD CANIDS: THE INFLUENCE OF DEVELOPMENT ON MORPHOLOGICAL CHANGE

The domestic dog varies remarkably in cranial morphology. In fact, the differences in size and proportion between some dog breeds are as great as those between many genera of wild canids. In this study, I compare patterns of intracranial allometry and morphologic diversity between the domestic dog and wild canid species. The results demonstrate that the domestic dog is morphologically distinct from all other canids except its close relatives, the wolf-like canids. Following this, I compare patterns of static and ontogenetic scaling. Data on growth of domestic dogs are presented and used to investigate the developmental mechanisms underlying breed evolution. Apparently, most small breeds are paedomorphic with respect to certain morphologic characters. In dogs and other domestic animals, morphologic diversity among adults seems to depend on that expressed during development.     

Speciation, phylogeography and evolution of life history and morphology in plethodontid salamanders of the Eurycea multiplicata complex

Understanding the complex interactions among environment, genotype and ontogeny in determining organismal phenotypes is cental to many biological disciplines. The Eurycea multiplicata complex, endemic to the Interior Highlands (Ozark Plateau and Ouachita Mountains) of eastern North America, comprises a diverse radiation of paedomorphic surface-dwelling (E. tynerensis), metamorphic surface-dwelling (E. multiplicata multiplicata and E. m. griseogaster) and metamorphic subterranean (Typhlotriton spelaeus) hemidactyliine plethodontid salamanders. Portions of two mitochondrial genes, cytochrome-b and NADH dehydrogenase-4, totalling 1818 base pairs (bp) were sequenced for 70 ingroup individuals plus numerous outgroup taxa, to examine the biogeography and relationships among these morphologically disparate species. Results show the E. multiplicata complex to be monophyletic, with its two most divergent clades corresponding to geography, not morphology or life history. Transforming surface-dwelling populations from the Ouachitas (E. m. multiplicata) are sister to the Ozark taxa, including paedomorphic surface-dwelling (E. tynerensis), subterranean (T. spelaeus) and transforming surface-dwelling salamanders assigned to the 'subspecies'E. m. griseogaster. Among Ozark taxa T. spelaeus (deeply nested within Eurycea) is sister to a clade that includes E. m. griseogaster and E. tynerensis. Current taxonomy suggests that paedomorphic populations (E. tynerensis) from the western Ozarks are distinct from nearby transforming populations (E. m. griseogaster). However, paedomorphic and transforming salamanders do not form reciprocally monophyletic groups and many populations share almost identical haplotypes. Ancestral state reconstruction of life history traits shows that paedomorphosis arose independently from three to nine times. Most populations are either completely paedomorphic or completely transforming. This suggests that local habitat parameters strongly influence life history mode in this complex, either facultatively or by selection for particular genotypes.     

Facultative paedomorphosis and the pattern of intra- and interspecific variation in cranial skeleton: lessons from European newts (Ichthyosaura alpestris and Lissotriton vulgaris)

Paedomorphosis, the presence of ancestral larval and juvenile traits that occur at the descendent adult stage, is an evolutionary phenomenon that shaped morphological evolution in many vertebrate lineages, including tailed amphibians. Among salamandrid species, paedomorphic and metamorphic phenotypes can be observed within single populations (facultative paedomorphosis). Despite wide interest in facultative paedomorphosis and polymorphism produced by heterochronic changes (heterochronic polymorphism), the studies that investigate intraspecific morphological variation in facultative paedomorphic species are largely missing. By quantifying the cranium size and development (bone development and remodeling), we investigated the variation at multiple levels (i.e., between sexes, populations and species) of two facultatively paedomorphic European newt species: the alpine and the smooth newt. The pattern of variation between paedomorphs (individuals keeping larval traits at the adult stage) and metamorphs (metamorphosed adult individuals) varied between species and among populations within a single species. The patterns of variation in size and skull formation appear to be more uniform in the alpine than in the smooth newt, indicating that developmental constraints differed between species (more pronounced in alpine than in smooth newt). Our study shows that the cranial skeleton provides detailed insight in the pattern of variation and divergence in heterochronic polymorphism within and between species and open new questions related to heterochronic polymorphism and evolution of cranial skeleton.     

Thyroid hormone responsive QTL and the evolution of paedomorphic salamanders

The transformation of ancestral phenotypes into novel traits is poorly understood for many examples of evolutionary novelty. Ancestrally, salamanders have a biphasic life cycle with an aquatic larval stage, a brief and pronounced metamorphosis, followed by a terrestrial adult stage. Repeatedly during evolution, metamorphic timing has been delayed to exploit growth-permissive environments, resulting in paedomorphic salamanders that retain larval traits as adults. We used thyroid hormone (TH) to rescue metamorphic phenotypes in paedomorphic salamanders and then identified quantitative trait loci (QTL) for life history traits that are associated with amphibian life cycle evolution: metamorphic timing and adult body size. We demonstrate that paedomorphic tiger salamanders (Ambystoma tigrinum complex) carry alleles at three moderate effect QTL (met1–3) that vary in responsiveness to TH and additively affect metamorphic timing. Salamanders that delay metamorphosis attain significantly larger body sizes as adults and met2 explains a significant portion of this variation. Thus, substitution of alleles at TH-responsive loci suggests an adaptive pleiotropic basis for two key life-history traits in amphibians: body size and metamorphic timing. Our study demonstrates a likely pathway for the evolution of novel paedomorphic species from metamorphic ancestors via selection of TH-response alleles that delay metamorphic timing and increase adult body size.     

The chromosomal complement of Aphia minuta, a paedomorphic goby

The diploid complement of the paedomorphic goby Aphia minuta ranged from 44 to 41 due to Robertsonian fusions (fundamental number=44). Data on spermatogenesis suggest that structural heterozygotes are fertile and that these chromosomal changes are not involved in a speciation process.