Development of the cranium and paired fins inBetta splendens (Teleostei: Percomorpha): Intraspecific variation and interspecific comparisons

Mabee, Paula M.; Trendler, Teresa A.

doi:10.1002/(sici)1097-4687(199603)227:3<249::aid-jmor1>3.0.co;2-1

Cited by 127 publications

(146 citation statements)

References 43 publications

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“…OSA has normally been used to understand variation and development in extant organisms (32,(56)(57)(58)(59)(60), with only a few previously published studies using this method in extinct taxa (21,61). We followed standard OSA procedure (32) to conduct this analysis.…”

Section: Methodsmentioning

confidence: 99%

Anomalously high variation in postnatal development is ancestral for dinosaurs but lost in birds

Griffin

Nesbitt

2016

Proc. Natl. Acad. Sci. U.S.A.

127

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Compared with all other living reptiles, birds grow extremely fast and possess unusually low levels of intraspecific variation during postnatal development. It is now clear that birds inherited their high rates of growth from their dinosaurian ancestors, but the origin of the avian condition of low variation during development is poorly constrained. The most well-understood growth trajectories of later Mesozoic theropods (e.g., Tyrannosaurus, Allosaurus) show similarly low variation to birds, contrasting with higher variation in extant crocodylians. Here, we show that deep within Dinosauria, among the earliest-diverging dinosaurs, anomalously high intraspecific variation is widespread but then is lost in more derived theropods. This style of development is ancestral for dinosaurs and their closest relatives, and, surprisingly, this level of variation is far higher than in living crocodylians. Among early dinosaurs, this variation is widespread across Pangaea in the Triassic and Early Jurassic, and among early-diverging theropods (ceratosaurs), this variation is maintained for 165 million years to the end of the Cretaceous. Because the Late Triassic environment across Pangaea was volatile and heterogeneous, this variation may have contributed to the rise of dinosaurian dominance through the end of the Triassic Period.I n comparison with other reptiles, avian biology is highly unusual, characterized by "hollow" bones and postcranial skeletal pneumaticity, feathers, a unique forelimb digit formula, endothermy, and rapid growth rates. However, these peculiarities initially arose in nonavian dinosaurs (1-7) in a gradual process occurring over tens of millions of years (8,9). In addition to their extremely rapid rates of growth, avian ontogeny possesses a characteristically low level of morphological variation within a species relative to that of other reptiles. The majority of individuals in a given avian species undergoes the same morphological changes during ontogeny in the same order at similar body sizes (10, 11), whereas their closest living relatives, crocodylians, possess higher variation (10,(12)(13)(14). How and when this feature of avian biology evolved is poorly constrained.This avian style of development must have evolved after its most recent common ancestor with crocodylians but before the origin of Aves. Most studies of the ontogeny of more-derived theropods (15-17) suggest that the low levels of variation that characterize avian ontogeny were present in close nonavian relatives as well. Closer to the origin of Dinosauria, morphological variation within species is widespread (18-26), but whether this variation is the result of taxonomic diversity, ontogeny, sexual dimorphism, or simple individual variation is not clear (22,23,27). Furthermore, close dinosaurian relatives or "dinosaur precursors" (e.g., Silesaurus, Asilisaurus) possess high intraspecific variation in growth sequences [i.e., sequence polymorphism (28)], suggesting that this condition could be ancestral for Dinosauria (21).In contrast to ...

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Section: Methodsmentioning

confidence: 99%

Anomalously high variation in postnatal development is ancestral for dinosaurs but lost in birds

Griffin

Nesbitt

2016

Proc. Natl. Acad. Sci. U.S.A.

127

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“…Functional needs have often been implicated in the ossification sequence of the teleostean skeleton (Vandewalle et al, 1992;Cubbage and Mabee, 1996;Mabee and Trendler, 1996). Bones involved in early functions such as respiration and feeding have generally been observed to ossify first.…”

Section: Ossification Sequence Of the Pharyngeal Jaw Apparatusmentioning

confidence: 99%

Embryonic Development and Skeletogenesis of the Pharyngeal Jaw Apparatus in the Cichlid Nile Tilapia (Oreochromis niloticus)

Pabic

Stellwag

Scemama

2009

The Anatomical Record

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The evolution of a specialized pharyngeal jaw apparatus (PJA) has been argued to be the key evolutionary innovation that allowed the explosive adaptive radiation of cichlid fishes in East African lakes. Subsequent studies together with recent molecular phylogenies have shown that similar innovations evolved independently several times within the teleosts, which poses the questions: (1) how similar are the developmental mechanisms responsible for these changes in divergent taxa and (2) how did such complex features arise independently in evolution? A detailed knowledge of PJA development in cichlids and other teleosts is needed to address these questions. Here, we provide a detailed account of the development of the PJA in one species of cichlid, the Nile tilapia (Oreochromis niloticus), from the early segmentation and patterning of its embryonic precursors -pharyngeal arches 3 to 7 -to its ossification. We find that pharyngeal segmentation occurs sequentially from anterior to posterior during early segmentation stages through the mid-pharyngula period. We show a clear combinatorial code of Hox gene expression such that each posterior arch is defined by a distinctive Hox signature. Posterior arch chondrogenesis in tilapia is essentially complete by the end of the hatching period, and most elements become ossified over the next two days. Our results reveal that both the fusion of lower jaw bones and articulation between the neurocranium and upper jaws occur during post-embryonic development. Abstract end data should be: Anat Rec, 292:1780Rec, 292: -1800Rec, 292: , 2009. V V C 2009 Wiley-Liss, Inc.

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“…Even fewer studies have been designed so that intraspecific variation in the relative sequence of developmental events can be assessed, although this variation must be the basis for evolutionary change. Intraspecific variation in developmental ossification sequences was documented from the zebrafish (Danio rerio) by Cubbage and Mabee (1996) and from the Siamese fighting fish (Betta splendens) by Mabee and Trendler (1996), but a quantitative analysis of the patterns within this variation was not made. Here, we quantify the effect of rearing temperature on the sequence of ossification and characterize the levels and patterns of intraspecific variation in these fishes.…”

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confidence: 99%

“…Individual species' sequences are compared with each other in evolutionary studies of heterochrony; the assumption is that the temporal sequence of events is invariant within a species (Alberch and Blanco 1996). This assumption is likely invalid because intraspecific variation in developmental ossification sequences has been documented from fishes (Cubbage and Mabee 1996;Mabee and Trendler 1996). These studies revealed variation in the relative timing of skull bone development in two species, Danio rerio, the zebrafish, and Betta splendens, the Siamese fighting fish.…”

mentioning

confidence: 99%

“…Thus, we analyzed the data on intraspecific variation reported for Betta (Mabee and Trendler 1996) to provide the basis for interspecific comparison. We examined the patterns and variation present in the sequence of skull development in both species with respect to bone embryology (cartilage vs. dermal), regional associations, functional importance, and association with the lateral line system, and whether a bone was median, paired, or iterated (repeated) in the cranium.…”

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confidence: 99%

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An Experimental Study of Intraspecific Variation, Developmental Timing, and Heterochrony in Fishes

2000

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Abstract. Heterochrony is widely regarded as an important evolutionary mechanism, one that may underlie most, if not all, morphological evolution, yet relatively few studies have examined variation in the sequence of development. Even fewer studies have been designed so that intraspecific variation in the relative sequence of developmental events can be assessed, although this variation must be the basis for evolutionary change. Intraspecific variation in developmental ossification sequences was documented from the zebrafish (Danio rerio) by Cubbage and Mabee (1996) and from the Siamese fighting fish (Betta splendens) by Mabee and Trendler (1996), but a quantitative analysis of the patterns within this variation was not made. Here, we quantify the effect of rearing temperature on the sequence of ossification and characterize the levels and patterns of intraspecific variation in these fishes. For Danio, there were no temperature effects on the sequence of bone development across the cranium, cranial region development, cartilage versus dermal bones, or lateral line bone versus nonassociated bones. Likewise the level of variation in relative sequence (position) of ossification was low, about two ranks, across temperatures. At higher temperatures, we found higher levels of variation in iterated cranial bones and less in bones forming early in the sequence. No temperature effects on variation were found among regions, between lateral line-associated bones and nonassociated bones, between median and paired bones, or across the entire sequence, indicating concordant variability among the three temperatures. Individual bones with the highest levels of variability were not consistent among temperatures.Baseline patterns of intraspecific variation in Danio were compared to those of Betta. For both species, the level of intraspecific variation in sequence position was low and the variability of cranial bones was concordant. Individual bones with the highest levels of variability were not consistent between species. In both species, variation was widespread (distributed evenly across the sequence). We used comparisons (among regions, between dermal and cartilage bones, between lateral line-associated and other bones, between median and paired bones, between iterated and noniterated bones, between feeding-associated bones and others) to see which subsets were most variable and thus potentially useful in predicting high levels of evolutionary change. The only subset of bones that was significantly more variable than others was cartilage bones. If interspecific patterns are parallel to these intraspecific differences, cartilage bones would be expected to show higher levels of heterochrony. Although concordance across the cranial ossification sequence and among regions in Danio, Betta, and two other teleosts, Oryzias and Barbus, suggests an evolutionarily conserved pattern of ossification, identity in sequence position across taxa was not observed for any bone. Thus, variation existed in sequence position across temperatures a...

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Development of the cranium and paired fins inBetta splendens (Teleostei: Percomorpha): Intraspecific variation and interspecific comparisons

Cited by 127 publications

References 43 publications

Anomalously high variation in postnatal development is ancestral for dinosaurs but lost in birds

Anomalously high variation in postnatal development is ancestral for dinosaurs but lost in birds

Embryonic Development and Skeletogenesis of the Pharyngeal Jaw Apparatus in the Cichlid Nile Tilapia (Oreochromis niloticus)

An Experimental Study of Intraspecific Variation, Developmental Timing, and Heterochrony in Fishes

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