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Quantitative Genetics of Larval Life-History Traits in a Myobatrachid Frog Crinia Georgiana Michael J

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Quantitative Genetics of Larval Life-History Traits in a Myobatrachid Frog Crinia Georgiana Michael J Animal Cells and Systems Vol. 16, No. 5, October 2012, 425Á430 Evolution under unpredictable environmental conditions: quantitative genetics of larval life-history traits in a myobatrachid frog Crinia georgiana Michael J. Smitha and Yikweon Jangb* aDepartment of Zoology, University of Western Australia, 35 Stirling Highway Crawley, Perth, Western Australia 6009, Australia; bDepartment of Life Sciences and Division of EcoScience, Ewha Womans University, Seoul, Republic of Korea (Received 1 March 2012; received in revised form 10 June 2012; accepted 19 July 2012) The southwestern Australian frog Crinia georgiana (Anura; Myobatrachidae) inhabits ephemeral pools in which the tadpoles often face desiccation. Under these conditions selection on tadpoles can be severe and can directly affect fitness during the aquatic as well as the terrestrial developmental stages. A quantitative genetic study using a half-sib breeding design was conducted to understand the genetic effects on larval life-history traits. We found no significant additive genetic variance in any of larval traits. Except for hatching period, heritability estimates based on females were high in egg size, larval period, snout-vent length, and weight at metamorphosis, suggesting non-additive genetic effects. These results indicate that any response to selection during hatching and larval periods should be predominately governed by non-additive genetic effects in C. georgiana. Keywords: additive genetic variation; larval period; maternal effect; multiple mating Introduction reproductive success and fecundity (Halliday and Natural selection favors those individuals whose traits Tejedo 1995). allow them to deal with unpredictable environmental Although the survival benefits of accelerated devel- conditions (Darwin 1871). In facing unpredictable opment are clear in the case of drying ponds, the genetic conditions, two strategies may be employed: (1) in- basis underlying such responses to selection pressures dividuals develop traits that enable them to avoid are still poorly understood. Quantitative genetic tech- unfavorable conditions until favorable circumstances niques are now commonly employed to reveal the return (e.g., hibernation; Holenweg and Reyer 2000) or amount of genetic variability in traits that are expressed during development and the genetic relationships (2) individuals develop traits that allow them to directly between these traits (Roff 1996, 1997; Collins et al. cope with the unfavorable conditions (e.g., accelerated 1998; Jang and Greenfield 2000; Dziminski et al. 2008). larval development to counteract pond drying; Abrams Considerable phenotypic variability in amphibian larval et al. 1996). traits has been detected, even in frog species that reside Dealing with unpredictable environmental condi- in permanent water bodies (Travis et al. 1987), and tions is especially important during early development subsequent quantitative genetic studies have detected because it can not only have a direct impact on fitness considerable additive genetic variation in these traits at the current life-history stage, but can also effect (Berven 1987; Newman 1988; Sommer and Pearman future development, survival, and fecundity (Semlitsch 2003). Additive genetic variation refers to the amount of et al. 1988; Berven 1990). For example, organisms that variation that is attributable to allelic differences between inhabit temporary pools are likely to have evolved in individuals (Falconer and Mackay 1996). Heritability, physiological, ontogenic, and behavioral responses to which is defined as additive genetic variance divided by the threat of desiccation such as the ability to accelerate phenotypic variance, determines the extent to which EVOLUTION & development to metamorphosis (Leips et al. 2000). SYSTEMATIC genetic differences contribute to differences in a pheno- BIOLOGY However, several potential costs associated with accel- typic trait (Falconer and Mackay 1996). erating development during the larval life-history stage In southwestern Australia, Crinia georgiana have been detected. In frogs, accelerating larval devel- (Anura; Myobatrachidae) inhabits temporary pools opment may lead to a smaller size at metamorphosis that are extremely variable in terms of size and which may influence the chances of surviving to duration (Doughty and Roberts 2003). Pair formation maturity during the terrestrial life-history stages (Smith in this species is characterized by male acoustic 1987) and affect the maturation phenotype such as size signaling and female phonotaxis (Gerhardt et al. and age at maturity (Altwegg and Reyer 2003). The 2000; Jang et al. 2011; Yoo and Jang 2012). However, maturation phenotype can in turn directly influence polyandrous matings often occur when intruding males *Corresponding author. Email: [email protected] ISSN 1976-8354 print/ISSN 2151-2485 online # 2012 Korean Society for Integrative Biology http://dx.doi.org/10.1080/19768354.2012.715594 http://www.tandfonline.com 426 M.J. Smith and Y. Jang join mating pairs (Byrne and Roberts 1999; Roberts kept under a 12:12 h light:dark photoperiod, and the et al. 1999). C. georgiana breeds during the winter temperature was maintained with an 18:158C cycle months (June to September) and deposits eggs in small between the light and dark photoperiod. The diet temporary pools where the larvae often face desicca- for tadpoles proportionally consisted of 3.5 parts of tion (Doughty 2002; Doughty and Roberts 2003). ‘‘Prepact’’ rabbit and guinea pig pellets, 1.5 parts of There is a high variability in egg size both within and ‘‘Tetramin Tropical Fish Food’’, and a tablet of ‘‘Bob between clutches, independent of female phenotype in Martin’’ vitamin and mineral supplement (Smith and C. georgiana, which may have evolved in response to Roberts 2003c). These diet components were ground the unpredictability in pond drying (Dziminski and and sieved through a 0.2-mm mesh. The tadpoles were Roberts, 2006). A quantitative genetic study found fed 10 mg of food twice every week until metamor- significant nonadditive genetic effects on larval fitness phosis. Water was changed weekly. traits, but no additive genetic effects were found on these traits (Dziminski et al. 2008). Eggs are usually laid in discrete clumps (Seymour and Roberts 1995), Genetic parameter estimation and tadpoles can survive to metamorphosis without For the half-sib breeding experiment, 27 males and feeding (Byrne and Roberts 2000). Thus, the natural 81 females were used for mating, and five eggs were history of C. georgiana suggests strong selection for randomly chosen from each mating. Twenty three rapid development. In this study, we investigated the tadpoles died during the course of the experiment: genetic basis of embryonic and larval life-history traits one tadpole from each of 19 full-sib families and two in the myobatrachid frog, C. georgiana using quantita- tadpoles from each of two full-sib families. Thus, the tive genetic techniques. Findings of this study are breeding experiment consisted of 81 full-sib families discussed within the context of adaptation to highly and 381 offspring (F ). variable and unpredictable environmental conditions. 1 Traits measured for estimation of genetic para- meters were egg size, hatching period, larval period, snout-vent length (SVL) at metamorphosis, and weight Materials and methods at metamorphosis. Egg size was measured with a Leica Population studied and experimental pairing MZ6 dissection microscope (9 0.01 mm) within 1.5 From 23 June to 3 July 2000 adult frogs were collected hours of fertilization. Each egg was placed in a Petri from two localities in southwestern Australia, Kangaroo dish with 70 ml of water. The egg was rotated and Gully and Boulder Rock, which were 3 km apart. The measured three times and the largest diameter was study areas were described thoroughly by Byrne and recorded. Hatching period was the number of days Roberts (1999, 2000), Roberts et al. (1999), Doughty from egg fertilization to hatching. Larval period was (2002), Doughty and Roberts (2003), Smith and Roberts the number of days from hatching to metamorphosis, (2003a, 2003b, 2003c), and Smith et al. (2003). At both which was defined as complete tail resorption (Gosner sites frogs breed in the numerous temporary shallow 1960). The metamorphs were gently blotted dry and pools (up to 30 cm deep) that form around the edge of weighed to the nearest milligram. Metamorphs were granite outcrops which are in turn surrounded by then placed under a plastic sheet with 0.01-mm grids eucalypt forests (Roberts et al. 1999). printed on it, and their SVLs were measured under a We used a half-sib breeding protocol (Becker 1984; Leica MZ6 dissection microscope. Falconer and Mackay 1996) to estimate genetic para- Because all traits were not severely deviated from meters. A male (sire) was mated with three randomly the normal distribution (skewness 5 0.96), untrans- selected female frogs (dam). The male was placed with formed values of traits were used for statistical analyses a female in a 500-ml plastic container with about 50 ml (see Table 1). A nested analysis of variance (ANOVA) of filtered and deionized water. Males were then washed down with water and similarly paired with Table 1. Descriptive statistics of the embryonic and larval the second and then the third female. The remating traits that were measured from Crinia georgiana. N381. time for males ranged from one hour to one day. No Mean SD Min Max male was kept in the lab for more than three days, and female frogs were only mated once. All pairs produced Egg size (mm) 2.168 0.1502 1.9 3.2 fertilized eggs within one hour. Hatching period (day) 13.33 1.709 3 21 Eggs were housed singly in 500-ml plastic contain- Larval period (day) 54.28 8.339 40 88 ers with 250 ml of filtered and deionized water until SVL at met. (mm) 6.845 0.6100 4.8 9.0 metamorphosis. The containers were placed into eight Weight at met. (g) 0.0310 0.0077 0.0112 0.0607 shelves in a randomized order. The rearing room was met., metamorphosis. Animal Cells and Systems 427 for unequal sample sizes was used (Sokal and Rohlf tailed t test with unequal variance) and weight 1995) to estimate genetic parameters.
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