Heterochrony and ecology in Jurassic and Cretaceous Ammonites
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Keywords:
Neoteny
Heterochrony
Ammonite
Ammonoidea
Begging
Abstract We have known since Trueman's classic work of 1922 that the Lower Jurassic Gryphaea of Britain exhibit phyletic size increase and heterochronic change in shape. Since Hallam's revisionary work in the 1960s, we have recognized that pronounced and generalized juvenilization of form accompanied this increasing size. This extensive literature provides invertebrate paleontology's most famous example of a biometrically documented, continuous anagenetic trend within a discrete lineage. But Gryphaea has also provoked great frustration because a key datum, required for a full solution, had been theoretically recognized but practically unavailable. We could identify the evolution of shape as paedomorphic, but could not specify the mode of heterochrony for this paedomorphic result because we could not standardize samples by common age or developmental stage. In this paper, we provide sclerochronological data on sizes and shapes at specified ages marked by annual growth bands in two Jurassic sequences of Gryphaea : the classic Lower Jurassic series showing phyletic size increase with paedomorphosis, and an independent Middle–Upper Jurassic series illustrating neither size increase nor heterochrony. We prove that size increase in the classic series occurs entirely by faster growth (larger descendant sizes at the same ages as ancestors), and not by extended age (for descendants lived no longer than ancestors). The well-marked paedomorphosis of form probably arose as a correlated consequence of growing larger by extending and maintaining rapid juvenile growth rates—thus marking the heterochronic mode as a case of neoteny. The independent upper sequence, acting as a different replicate in a natural experiment, shows neither size increase nor heterochrony but does exhibit (in contrast with the classic sequence) evolution toward greater longevity. Hallam's flow tank experiments indicated a strong adaptive advantage in shell stability for both larger size and paedomorphic form. Neotenous development provides an evolutionary pathway to the simultaneous acquisition of both favored traits—thus showing that “constraints” due to “correlations of growth” (Darwin's own phrase for the phenomenon) may be positive in promoting joint evolutionary advantages, and not only neutral (in carrying spandrels along with primary adaptations), or negative (by imposing inadaptive “baggage” upon trends in form through developmental correlation with selected traits).
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Phyletic gradualism
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Astogenetic trajectories have constrained evolutionary changes in bryozoans. Rates and timing of astogenetic differentiation have been modified for characters defining the morphology of zooids, subcolonies, and colonies. This paper catalogs 46 examples of bryozoan heterochrony, representing all five skeletonized orders. Heterochrony is inferred to have been a pervasive phenomenon in the evolution of Paleozoic stenolaemates, illustrated by 40 examples, 19 of which produced paedomorphosis and 21 peramorphosis. As a consequence, a restricted range of morphologic states has reappeared repetitively as homeomorphies and evolutionary reversals. Large-scale patterns developed across both geologic time and geographic space reflect variation in heterochronic products irrespective of the developmental processes by which they were achieved. Available evidence indicates that smaller, paedomorphic, and more plastic species inhabited onshore, low-diversity areas. Nonheritable plasticity is inferred to be a correlate of early growth stages and paedomorphosis. Taller, generally peramorphic species with damped plasticity are found in higher diversity, offshore regions. Seven key innovations, which first appeared during the early diversification of bryozoan clades, are peramorphic, and recapitulation was a predominant pattern during their Ordovician radiation. Trends in later phylogeny, on the other hand, have favored paedomorphic derived morphologies, as illustrated by 19 of the 32 examples. Recurrent reverse recapitulation suggests that offshore ancestors frequently gave rise to onshore paedomorphs.
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The reticuloceratid ammonoid Arkanites relictus (Quinn, McCaleb, and Webb, 1962) is represented by hundreds to thousands of individuals from horizons isolated both stratigraphically and geographically in northern Arkansas. These assemblages appear to represent mass mortality events resulting from a semelparous reproductive strategy. Arkanites relictus occurs as a dimorphic pair (depressed, widely umbilicate, cadiconic conchs and compressed, narrowly umbilicate, pachyconic conchs) thought to reflect sexual dimorphism. Late stage ontogenetic modifications, such as septal crowding and change in aperture profile, are widely cited evidence of sexual maturity in ammonoids. Septal crowding begins at a predictable ontogenetic stage in the compressed forms of A. relictus, but specimens with cadiconic conchs do not have crowded septa even at the largest diameters available. Depending on the trait examined and the proxy for age of individuals, the dimorphism in Arkanites relictus (using the depressed form as the reference morph) is the result of acceleration, neoteny, or hypermorphosis plus neoteny. If size (diameter) is considered a proxy for age, the dimorphs were the same age at death, and the septa in the compressed variants developed via acceleration relative to the depressed variants. Regarding conch shape (width vs. diameter), the compressed morphs developed via neoteny relative to the depressed morphs. If septal count is considered a proxy for age, the dimorphs were not the same age at death, and the compressed forms were produced by a combination of hypermorphosis plus neoteny, i.e., they grew longer yet slower than the depressed forms. In A. relictus, the heterochronic processes of hypermorphosis and neoteny may have been operating simultaneously, which is an interesting possibility because it is an example of a combination of both peramorphic and paedomorphic processes.
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The reticuloceratid ammonoid Arkanites relictus (Quinn, McCaleb, and Webb, 1962) is represented by hundreds to thousands of individuals from horizons isolated both stratigraphically and geographically in northern Arkansas. These assemblages appear to represent mass mortality events resulting from a semelparous reproductive strategy. Arkanites relictus occurs as a dimorphic pair (depressed, widely umbilicate, cadiconic conchs and compressed, narrowly umbilicate, pachyconic conchs) thought to reflect sexual dimorphism. Late stage ontogenetic modifications, such as septal crowding and change in aperture profile, are widely cited evidence of sexual maturity in ammonoids. Septal crowding begins at a predictable ontogenetic stage in the compressed forms of A. relictus, but specimens with cadiconic conchs do not have crowded septa even at the largest diameters available.Depending on the trait examined and the proxy for age of individuals, the dimorphism in Arkanites relictus (using the depressed form as the reference morph) is the result of acceleration, neoteny, or hypermorphosis plus neoteny. If size (diameter) is considered a proxy for age, the dimorphs were the same age at death, and the septa in the compressed variants developed via acceleration relative to the depressed variants. Regarding conch shape (width vs. diameter), the compressed morphs developed via neoteny relative to the depressed morphs. If septal count is considered a proxy for age, the dimorphs were not the same age at death, and the compressed forms were produced by a combination of hypermorphosis plus neoteny, i.e., they grew longer yet slower than the depressed forms. In A. relictus, the heterochronic processes of hypermorphosis and neoteny may have been operating simultaneously, which is an interesting possibility because it is an example of a combination of both peramorphic and paedomorphic processes.
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Heterochrony
Sexual dimorphism
Ammonoidea
Conch
Sexual maturity
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Neoteny
Heterochrony
Ammonite
Ammonoidea
Begging
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This paper reviews Gould's clock model for heterochronic processes and uses that model to develop simple matrix representations of growth and shape change. Matrix representations of growth and development provide a common formulation for all heterochronic processes. In particular, we show how neoteny can be diagnosed using such a matrix approach. The literature is rife with contradictory representations of how neoteny affects growth allometries and the timing of developmental events, and therefore of the role of neoteny in human evolution. Through the use of multivariate models, we explore these relationships and the internal consistency of opposing views. Gould's neoteny hypothesis for human evolution has been criticized for a number of reasons. Humans do not grow slowly. The slopes of our growth allometries show no common pattern of change vis-a-vis those of our closest relatives. Humans prolong rather than reduce rates of growth and development of body parts; the brain, for example, ceases growing later in humans than in apes, but during this prolonged period of early ontogeny, it grows at a rapid pace. This paper evaluates Gould's hypothesis and its critiques by focusing on particular questions. Does neoteny imply slow growth? Does it imply a unidirectional change in the rates of growth of traits? Under neoteny, should the brain cease growing in ancestor and descendant at the same age? Does prolongation of phases of growth and development confute neoteny? On the other hand, is paedomorphosis an inevitable consequence of prolonged growth and development? We show that, for all of these questions, the answer is no. © 1996 Wiley-Liss, Inc.
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Hominidae
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The writer discusses the problem, suggested by some authors, of interpretation of small forms in Ammonoidea as neotenic ones. The classical conception of neoteny is connected with presence of a larval stage which in Ammonoidea was very tiny. It therefore appears that small forms in Ammonoidea are highly advanced in their ontogenetic development as compared with a larval stage of this group. Numerous examples are also known of the dimorphism, the large and small forms in which differ in their dimensions very indistinctly. The latter facts contradict a conception of a neotectonic character of small forms. The writer discusses also the problem of systematics of the Ammonoidea against the background of the commonly being accepted theory of sexual dimorphism.
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Non-avian saurischian skulls underwent at least 165 million years of evolution and shapes varied from elongated skulls, such as in Coelophysis , to short and box-shaped skulls, such as in Camarasaurus . A number of factors have long been considered to drive skull shape, including phylogeny, dietary preferences and functional constraints. However, heterochrony is increasingly being recognized as a major factor in dinosaur evolution. In order to quantitatively analyse the impact of heterochrony on saurischian skull shape, we have analysed five ontogenetic trajectories using two-dimensional geometric morphometrics in a phylogenetic framework. This allowed for the evaluation of how heterochrony affected overall skull shape through both ontogenetic and phylogenetic trajectories and how it impacted modular changes within the skull. Using principal component analyses and multivariate regressions, it was possible to quantify different ontogenetic trajectories in light of heterochrony. The results recovered here indicate that taxa underwent a combination of local paedomorphosis and peramorphosis within the skull along individual ontogenies and phylogenies, but that either peramorphosis or paedomorphosis dominated when the skull was considered as a whole. We found that the hypothetical ancestor of Saurischia led to basal Sauropodomorpha mainly through paedomorphosis, and to Neotheropoda mainly through peramorphosis. Paedomorphosis then led from Orionides to Avetheropoda, indicating that the paedomorphic trend previously found in advanced coelurosaurs may extend back into the early evolution of Avetheropoda. Not only are changes in saurischian skull shape complex due to the large number of factors that affect shape, but heterochrony itself is complex, with a number of reversals throughout non-avian saurischian evolution. The sampling of ontogenetic trajectories is considerably lower than the sampling of adult species and the current study represents a first exploratory analysis. To better understand the impact of heterochrony on cranial evolution in saurischians, the data set we present must be expanded and complemented with further sampling from future fossil discoveries, especially of juvenile taxa.
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Postcrania
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