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Local Adaptation, Countergradient Variation and Ecological Genetics of Life-history Traits in Rana Temporaria
Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology, Population Biology.
2003 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The main aim of this work was to identify local adaptation processes in amphibian populations, thereby improving the general understanding of genetics and mechanisms behind the evolution and maintenance of biological diversity. Phenotypic and genetic variation in life-history traits was studied within and between populations common frog (Rana temporaria) populations along a 1600 km transect from southern Sweden to northern Finland.

Embryonic and larval development and growth was investigated both under field and laboratory conditions. The results suggest ample genetic diversity in larval life-history traits among Fennoscandian common frog populations. Larval developmental rate along the gradient has evolved a countergradient variation pattern of genotypes and phenotypes as indicated by the positive relationship between developmental rate and latitude under laboratory conditions and the lack of such a relationship in the field. The data suggest that this pattern has evolved because of time constraints due to decreasing length of growth season with latitude. Neither field-caught adults nor laboratory raised larvae displayed a linear latitudinal size cline as expected from the so called Bergmanns rule. Rather, size increased towards the mid-latitude populations and decreased thereafter, indicating that body size is a product of direct environmental induction or a trade-off with other life-history characters. Age and size at hatching showed no consistent latitudinal pattern, indicating that the embryonic stage is not as time constrained as the larval stage.

A large part of the variation in age and size at metamorphosis among populations was due to additive genetic effects. However, small, but significant maternal effects, mostly due to variation in egg size and non-additive genetic effects also contributed to among population variation. A comparison of divergence in presumably neutral molecular genetic markers (FST) and quantitative characters (QST) revealed that although both estimates of divergence were relatively high, estimates of QST was generally higher than those of FST, indicating that the genetic variation observed in larval traits is primarily a result of natural selection rather than genetic drift. Hence, our results reinforce the conclusion that intraspecific genetic heterogeneity in the young northern European ecosystems may be more widespread than previously anticipated

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis , 2003. , p. 33
Series
Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1104-232X ; 818
Keyword [en]
Ecology, amphibians, Bergmanns rule, body size clines, countergradient variation, developmental rate, FST, temperature, QST
Keyword [sv]
Ekologi
National Category
Ecology
Research subject
Population Biology
Identifiers
URN: urn:nbn:se:uu:diva-3332ISBN: 91-554-5558-1 (print)OAI: oai:DiVA.org:uu-3332DiVA, id: diva2:162414
Public defence
2003-03-28, Zootissalen, Uppsala, 13:00
Opponent
Available from: 2003-03-06 Created: 2003-03-06Bibliographically approved
List of papers
1. Latitudinal and temperature-dependent variation in embryonic development and growth in Rana temporaria
Open this publication in new window or tab >>Latitudinal and temperature-dependent variation in embryonic development and growth in Rana temporaria
2003 (English)In: Oecologia, ISSN 0029-8549, E-ISSN 1432-1939, Vol. 135, no 4, p. 548-554Article in journal (Refereed) Published
Abstract [en]

Variation in seasonal time constraints and temperature along latitudinal gradients are expected to select for life history trait differentiation, but information about the relative importance of these factors in shaping patterns of divergence in embryonic traits remains sparse. We studied embryonic survival, growth and development rates in the common frog (Rana temporaria) along a 1,400-km latitudinal gradient across Sweden by raising embryos from four populations in the laboratory at seven temperatures (9 degrees C, 12 degrees C, 15 degrees C, 18 degrees C, 21 degrees C, 24 degrees C, 27 degrees C). We found significant differences in mean values of all traits between the populations and temperature treatments, but this variation was not latitudinally ordered. In general, embryonic survival decreased at the two highest temperatures in all populations, but less so in the southernmost as compared to the other populations. The northernmost population developed slowest at the lowest temperature, while the two mid-latitude populations were slowest at the other temperatures. Hatchling size increased with increasing temperature especially in the two northern populations, whereas the two southern populations showed peak hatchling size at 15 degrees C. Analyses of within-population genetic variation with a half-sib design revealed that there was significant additive genetic variation in all traits, and egg size-related maternal effects were important in the case of hatchling size. Overall, our results indicate that unlike larval growth and development, variation in embryonic development and growth in R. temporaria cannot be explained in terms of a latitudinal gradient in season length. While adaptation to a latitudinal variation in temperature might have contributed to the observed differentiation in embryonic performance, the effects of other, perhaps more local environmental factors, seem to have overridden them in importance.

National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-90158 (URN)10.1007/s00442-003-1229-0 (DOI)16228254 (PubMedID)
Available from: 2003-03-06 Created: 2003-03-06 Last updated: 2017-12-14Bibliographically approved
2. Latitudinal countergradient variation in the common frog (Rana temporaria) developmental rates: evidence for local adaptation
Open this publication in new window or tab >>Latitudinal countergradient variation in the common frog (Rana temporaria) developmental rates: evidence for local adaptation
2003 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 16, no 5, p. 996-1005Article in journal (Refereed) Published
Abstract [en]

Adaptive genetic differentiation along a climatic gradient as a response to natural selection is not necessarily expressed at phenotypic level if environmental effects on population mean phenotypes oppose the genotypic effects. This form of cryptic evolution--called countergradient variation--has seldom been explicitly demonstrated for terrestrial vertebrates. We investigated the patterns of phenotypic and genotypic differentiation in developmental rates of common frogs (Rana temporaria) along a ca. 1600 km latitudinal gradient across Scandinavia. Developmental rates in the field were not latitudinally ordered, but displayed large variation even among different ponds within a given latitudinal area. In contrast, development rates assessed in the laboratory increased strongly and linearly with increasing latitude, suggesting a genetic capacity for faster development in the northern than the southern larvae. Experiments further revealed that environmental effects (temperature and food) could easily override the genetic effects on developmental rates, providing a possible mechanistic explanation as to why the genetic differentiation was not seen in the samples collected from the wild. Our results suggest that the higher developmental rates of the northern larvae are likely to be related to selection stemming from seasonal time constrains, rather than from selection dictated by low ambient temperatures per se. All in all, the results provide a demonstration of environmental effects concealing substantial latitudinally ordered genetic differentiation understandable in terms of adaptation to clinal variation in time constrains.

National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-90159 (URN)10.1046/j.1420-9101.2003.00560.x (DOI)14635915 (PubMedID)
Available from: 2003-03-06 Created: 2003-03-06 Last updated: 2017-12-14Bibliographically approved
3. Do common frogs (Rana temporaria) follow Bergmann’s rule?
Open this publication in new window or tab >>Do common frogs (Rana temporaria) follow Bergmann’s rule?
Show others...
2005 (English)In: Evolutionary Ecology Research, ISSN 1522-0613, E-ISSN 1937-3791, Vol. 7, no 5, p. 717-731Article in journal (Refereed) Published
Abstract [en]

Questions: Does intraspecific extension of Bergmanns rule – larger size within a species incooler areas – hold true for ectotherms in general, and for the common frog (Rana temporaria)in particular? What is the relative importance of genetic and environmental factors (i.e. directenvironmental induction) in determining latitudinal patterns of body size variation in commonfrogs?Methods: We tested for a positive association between mean body size and latitude incommon frogs (Rana temporaria) across a 1600 km long latitudinal gradient in Scandinaviaboth for wild-collected adults and laboratory-reared metamorphs.Results: In adults, the mean body size increased from south to mid-latitudes, and declinedthereafter. This occurred despite the fact that the mean age of adult frogs increased withincreasing latitude, and age and body size were positively correlated. The latitudinal pattern ofbody size variation in metamorphs reared in a common garden experiment was similar to thatobserved among wild-caught adults.Conclusions: The results suggest that the concave pattern of body size variation across thelatitudinal cline may be at least partly genetically determined, and that although there isconsiderable geographic variation in mean body size of R. temporaria, this variation does notconform with Bergmann’s rule.

Keyword
age, amphibians, body size, cline, growth, latitude, temperature
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-90160 (URN)
Available from: 2003-03-06 Created: 2003-03-06 Last updated: 2017-12-14Bibliographically approved
4. Maternal and genetic contributions to geographical variation in Rana temporaria larval life-history traits
Open this publication in new window or tab >>Maternal and genetic contributions to geographical variation in Rana temporaria larval life-history traits
2002 (English)In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 76, no 1, p. 61-70Article in journal (Refereed) Published
Abstract [en]

The relative importance of genetic, environmental, and maternal effects as determinants of geographical variation in vertebrate life-histories has not often been explored. We examined the role of genetic and maternal effects as determinants of population divergence in survival and three important larval life-history traits (growth rate, age, and size at metamorphosis) using reciprocal crosses between two latitudinally separated populations of the common frog (Rana temporaria Linnaeus). Genetic effects were important in all three traits as indicated by the significant effect of male origin, but there was also evidence for nonadditive genetic contributions on metamorphic size and growth rate. Likewise, maternal effect contributions to population divergence were large, partially environment dependent, and apparently acting primarily through egg size in two of three traits. These results suggest that both genetic and maternal effects are important determinants of geographical variation in amphibian life-histories, and that much of the differentiation resulting from maternal effects is mediated through variation in egg size.

National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-90161 (URN)10.1111/j.1095-8312.2002.tb01714.x (DOI)
Available from: 2003-03-06 Created: 2003-03-06 Last updated: 2017-12-14Bibliographically approved
5. Latitudinal divergence of common frog (Rana temporaria) life-history traits by natural selection: evidence for a comparison of molecular and quantitative genetic data
Open this publication in new window or tab >>Latitudinal divergence of common frog (Rana temporaria) life-history traits by natural selection: evidence for a comparison of molecular and quantitative genetic data
Show others...
2003 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 12, no 7, p. 1963-1978Article in journal (Refereed) Published
Abstract [en]

The relative roles of natural selection and direct environmental induction, as well as of natural selection and genetic drift, in creating clinal latitudinal variation in quantitative traits have seldom been assessed in vertebrates. To address these issues, we compared molecular and quantitative genetic differentiation between six common frog (Rana temporaria) populations along an approximately 1600 km long latitudinal gradient across Scandinavia. The degree of population differentiation (QST approximately 0.81) in three heritable quantitative traits (age and size at metamorphosis, growth rate) exceeded that in eight (neutral) microsatellite loci (FST = 0.24). Isolation by distance was clear for both neutral markers and quantitative traits, but considerably stronger for one of the three quantitative traits than for neutral markers. QST estimates obtained using animals subjected to different rearing conditions (temperature and food treatments) revealed some environmental dependency in patterns of population divergence in quantitative traits, but in general, these effects were weak in comparison to overall patterns. Pairwise comparisons of FST and QST estimates across populations and treatments revealed that the degree of quantitative trait differentiation was not generally predictable from knowledge of that in molecular markers. In fact, both positive and negative correlations were observed depending on conditions where the quantitative genetic variability had been measured. All in all, the results suggest a very high degree of genetic subdivision both in neutral marker genes and genes coding quantitative traits across a relatively recently (< 9000 years) colonized environmental gradient. In particular, they give evidence for natural selection being the primary agent behind the observed latitudinal differentiation in quantitative traits.

National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-90162 (URN)10.1046/j.1365-294X.2003.01865.x (DOI)12803645 (PubMedID)
Available from: 2003-03-06 Created: 2003-03-06 Last updated: 2017-12-14Bibliographically approved

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