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

Abstract

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...

Developmental stages until hatching of the Lake Victoria cichlid Haplochromis piceatus (Teleostei: Cichlidae)

“…Heterochrony and its biological implications have been considered extensively elsewhere (Gould, 1977;Richardson, 1995;Klingenberg, 1998;Richardson, 1999;Mabee et al, 2000;Smith, 2001;Jeffery et al, 2002;Richardson and Oelschä ger, 2002). Jones (1974) noted that heterochrony causes problems in comparison between different substrate brooding cichlid species and species hybrids.…”

Dynamic skeletogenesis in fishes: Insight of exercise training on developmental plasticity

“…However, developmental plasticity has been tested experimentally on a variety of species, phenotypes, and environmental factors. Phenotypic plasticity has been primarily studied in teleosts [e.g., adrianichthyid (Kawajiri et al, 2011), anarhichadids (Pavlov and Moksness, 1994), cichlids (Crispo and Chapman, 2010), clupeids (Fuiman et al, 1998), cyprinids (Mabee et al, 2000), gasterosteids (Garduno-Paz et al, 2010), moronids (Georgakopoulou et al, 2007), salmonids (Pakkasmaa and Piironen, 2001;Peres-Neto and Magnan, 2004;Grü nbaum et al, 2007Grü nbaum et al, , 2008Fischer-Rousseau et al, 2009;Cloutier et al, 2010;Totland et al, 2011)] most likely owing to the facility of rearing experiences; however, there is no a priori reason to think that it is limited to teleosts.…”

“…Although thermally induced plasticity has been highly documented Moksness, 1994, 1997;Fuiman et al, 1998;Mabee et al, 2000;Georgakopoulou et al, 2007;Schmidt and Starck, 2010;Kawajiri et al, 2011), numerous environmental/experimental factors have also been investigated such as dissolved oxygen (Schmidt and Starck, 2010), salinity (Schmidt and Starck, 2010), diet (Meyer, 1987;Huysseune et al, 1994;Muschick et al, 2011), predator odors (Frommen et al, 2011), hormonal conditions (Shkil et al, 2010), habitat heterogeneity (Garduno-Paz et al, 2010), and water velocity (Pakkasmaa and Piironen, 2001;PeresNeto and Magnan, 2004;Grü nbaum et al, 2007Grü nbaum et al, , 2008Cloutier et al, 2010;Totland et al, 2011). Water velocity is of primary interest for at least two reasons.…”

“…A wide range of plastic responses has been reported in the literature. Focusing on anatomical plasticity, the following traits exemplify the types of responses: size [e.g., gills (Crispo and Chapman, 2010), brain (Crispo and Chapman, 2010), head (Meyer, 1987), body (Pakkasmaa and Piironen, 2001;Peres-Neto and Magnan, 2004;Georgakopoulou et al, 2007;Grü nbaum et al, 2008;Schmidt and Starck, 2010;Frommen et al, 2011;Kawajiri et al, 2011), fins (Fischer-Rousseau et al, 2009)] and shape changes [e.g., head (Meyer, 1987), pharyngeal (Muschnick et al, 2011) and oral jaws (Meyer, 1987), body (Pakkasmaa and Piironen, 2001;Peres-Neto and Magnan, 2004;Georgakopoulou et al, 2007;Grü nbaum et al, 2007;Fischer-Rousseau et al, 2009;Garduno-Paz et al, 2010;Frommen et al, 2011)], bone matrix (Totland et al, 2011), number of serially repeated elements [e.g., pharyngeal teeth, vertebrae, fin rays, spines (Arratia and Schultze, 1992;Mabee et al, 2000;Georgakopoulou et al, 2007;Shkil et al, 2010;Kawajiri et al, 2011)], and timing of ossification Moksness, 1994, 1997;Fuiman et al, 1998;Mabee et al, 2000;Cloutier et al, 2010, Fiaz et al, 2012. It is also known that fin positioning is plastic with respect to changes in hydrodynamic conditions …”

Life history as a constraint on plasticity: developmental timing is correlated with phenotypic variation in birds

“…That is, we assume that a shift in flight timing by a few days results in a shift of timing of information but that the relative maturity of that trait at that point in time is comparable. However, heterochronic shifts are common across populations and species (Raff and Wray, 1989;Klingenberg, 1998;Smith, 2001) and the relative timing of trait development is itself plastic, varying with nutrition and temperature (Strathmann et al, 1992;Miller and German, 1999;Mabee et al, 2000). For instance, the relative timing of bone ossification differs across populations of finches (Badyaev et al, 2008) and species of mammals (Smith, 2006).…”