First evidence for postzygotic reproductive isolation between two populations of Eurasian perch (Perca fluviatilis L.) within Lake Constance
© Behrmann-Godel and Gerlach; licensee BioMed Central Ltd. 2008
Received: 23 April 2007
Accepted: 24 January 2008
Published: 24 January 2008
The evolution of reproductive traits, such as hybrid incompatibility (postzygotic isolation) and species recognition (prezygotic isolation), have shown their key role in speciation. Theoretical modeling has recently predicted that close linkage between genes controlling pre- and postzygotic reproductive isolation could accelerate the conditions for speciation. Postzygotic isolation could develop during the sympatric speciation process contributing to the divergence of populations. Using hybrid fitness as a measure of postzygotic reproductive isolation, we empirically studied population divergence in perch (Perca fluviatilis L.) from two genetically divergent populations within a lake.
During spawning time of perch we artificially created parental offspring and F1 hybrids of the two populations and studied fertilization rate and hatching success under laboratory conditions. The combined fitness measure (product of fertilization rate and hatching success) of F1 hybrids was significantly reduced compared to offspring from within population crosses.
Our results suggest intrinsic genetic incompatibility between the two populations and indicate that population divergence between two populations of perch inhabiting the same lake may indeed be promoted by postzygotic isolation.
One of the central issues of evolutionary debate is whether or not reproductive isolation, which is a prerequisite for any speciation process, can evolve in the absence of physical barriers to gene flow [1–4]. Many theoretical models predict that speciation occurs under sympatric and parapatric conditions [2, 5]. The most common models that try to explain sympatric speciation are either based on habitat-race formation, driven by habitat specific deleterious or beneficial alleles [1, 6], or on sexual selection, based on assortative mating [7, 8]. Disruptive selection among ecotypes followed by assortative mating could result in reduced gene flow between populations [9–14].
There is empirical evidence for the evolution of reproductive isolation under sympatric conditions [3, 15–19], however, sympatric speciation remains difficult to prove because reproductive isolation could as well have originated during an allopatric period, followed by secondary contact and introgression (, but see  and citations herein). To investigate mechanisms of premating isolation under sympatric conditions, Servedio  modeled increased linkage between genes controlling traits associated with mate recognition and genes controlling hybrid incompatibilities. She demonstrated that hybrid incompatibilities may develop under circumstances of increased linkage despite some gene flow and state that "postzygotic isolation may build up during the sympatric speciation process, accelerating and easing the conditions for speciation to proceed".
Rice and Hostert  showed that hybrids of two ecotypes can suffer reduced fitness, both because they may fall between distinct ecological niches of their parental populations and be selected against (extrinsic postzygotic isolation), and/or because of genetic incompatibilities between the parental populations (intrinsic postzygotic isolation). Negative epistatic effects have been shown to reduce hybrid fitness if populations that have diverged in allopatry meet again secondarily [23–25]. This could be explained by the Dobzhansky-Muller model [26, 27]. In the Dobzhansky-Muller model, hybrid sterility and inviability develop as pleiotropic byproducts during independent allopatric divergence of populations. Thereby substitutions, which have accumulated during allopatry and are neutral or beneficial in the genetic background of one population or species, are deleterious in hybrids when the species meet secondarily.
Schluter , Hatfield and Schluter  and Rundle  tested whether extrinsic and/or intrinsic postzygotic isolation played a role in stickleback speciation. They showed that F1 hybrids and backcrosses of sympatric populations of sticklebacks, a benthic and a limnetic form, had lower growth rates in both parental habitats. These results were regarded as an indication that extrinsic postzygotic isolation can occur. Intrinsic postzygotic isolation was negligible for both populations of sticklebacks.
Lake Constance is a very young prealpine lake, covering an area of 536 km2 that has formed at the end of the last Pleistocene glaciations . The earliest colonization by perch could thus have occurred 15 000 – 10 000 ybp . Perch from the two putative glacial refuges of Lake Constance, the Danube and Rhine rivers, differ in their mtDNA D-loop sequences . To investigate if genetic differentiation of perch from Lake Constance was due to multiple colonization from these two Pleistocene refuges, Behrmann-Godel et al.  sequenced 365 bp of the 5'end of the mtDNA D-loop. Almost exclusively Danube haplotypes were found within both populations, Rhine haplotypes also occurred in both populations but in very low frequencies. However, no significant population sub-structuring could be observed.
Here we analyze if postzygotic reproductive isolation occurs between the two perch populations of Lake Constance. We tested F1 hybrid crosses of both populations for the combined fitness parameters, fertilization rate and hatching success, to investigate whether intrinsic postzygotic isolation could contribute to divergence between these perch populations.
Various fitness parameters for parental and hybrid crosses
Number of females
Number of eggs
F 1 1
F 1 2
Fertilization success of eggs differed within our four experimental groups (Table 1, ANOVA on arcsine square root of proportions, F3,23 = 4.86, P = 0.009). F12 hybrids had a significantly lower egg fertilization rate as compared to all other crosses (eastern pop, 95%; western pop, 99%, F11, 99%, F12, 56%; linear contrast analysis, F1,23 = 14.29, P = 0.001). The hatching success did not differ significantly between crosses (Table 1, ANOVA on arcsine square root of proportions, F3,23 = 2.14, P = 0.122).
Six out of nine F12 hybrid crosses were conducted under laboratory conditions. This method may have resulted in reduced hybrid fitness of these particular crosses. However, a statistical analysis excluding these crosses did not alter our results. The CFM between crosses were still significantly different (ANOVA on arcsine square root of proportions, F3,17 = 3.60, P = 0.035) and hybrids still had a significantly lower CFM than parental crosses (linear contrast analysis, F1,17 = 7.13, P = 0.016 whereas there was no significant difference in the CFM, neither between the two parental crosses (linear contrast analysis, F1,17 = 2.82, P = 0.11) nor between the two hybrid crosses (linear contrast analysis, F1,17 = 0.12, P = 0.74).
Our results show reduced hybrid fitness in crosses of two genetically divergent populations of perch in Lake Constance which only differ by a mean FST value of 0.07
Both types of hybrid crosses had significantly lower CFM values than the within population crosses indicating intrinsic postzygotic isolation. This could be based on an acceleration of Dobzhansky- Muller's rate of incompatibilities [26, 27] by divergent selection which is generally believed to be the basis of most intrinsic genetic incompatibilities [39–41].
The slight differences (approx. one to two weeks) in the peak spawning times of the two populations could have resulted in crossing early and late breeders in the hybrid but not in the parental crosses. Early and late breeders within populations may be adapted to specific seasonal conditions and their hybrids may therefore exhibit outbreeding depression . However, we do not think that this explains the differences found in CFM values. In our hybrid crosses, all females were caught during peak spawning of their respective population (see methods section). The reproductive period of male perch exceed that of females. Males of both populations held in captivity stay ripe and running and can inseminate eggs from multiple females over a time period of two weeks before and after the main peak spawning time (Behrmann-Godel, personal observation). Therefore, reduced CFM values of hybrid crosses could not have been caused by not yet ripe or already depleted males.
Since we have no further data to clarify whether the observed reduced hybrid fitness evolved in sympatry, parapatry or allopatry, we suggest that the two populations of perch may have diverged during or at the end of the last ice age, which can be dated to 115 000 to 10 000 ybp . This seems a surprisingly short time span for genetic incompatibilities to evolve. Russell  and Bolnick and Near  have shown that hybrid viability declined with the time separating pairs of different fish species. Based on a Centrarchid phylogeny, calculations of Bolnick and Near  revealed that it takes approx. 5–10 my before the hatching compatibility of interspecific crosses starts to decrease. Similar results have been found for species pairs of darters (Percidae: Etheostoma)  and also for bird species , but Price and Bouvier could also show that hybrid infertility arises much earlier (in the order of a few million years). However, at least for allopatric Drosophila sister species, mathematical modeling shows that hybrid sterility and inviability evolve fast enough (in the order of thousands of years, assuming single incompatibility speciation) to contribute to speciation .
Our results on reduced hybrid fitness in perch are supported by findings of Lu and Bernatchez  and Rogers and Bernatchez  who showed that intrinsic and extrinsic postzygotic reproductive isolation in lake whitefish (Coregonus culpeaformis) could promote speciation. In hybrid-parental backcrosses between two allopatric populations of whitefish, Rogers and Bernatchez  found increased embryonic mortality and asynchrony in the developmental time to emergence of backcrosses. This indicated both, intrinsic and extrinsic mechanisms contributing to the formation and maintenance of reproductive isolation between lake whitefish populations that have diverged during the last Pleistocene glaciations, 18 000 to 50 0000 ybp, which is a quite comparable time span to the divergence time we suggested for the two perch populations of Lake Constance.
Coyne and Orr  showed that in Drosophila sister species prezygotic sexual isolation is stronger than postzygotic isolation, and that in sympatric species prezygotic isolation is greatly enhanced in comparison to allopatric species. We might expect to find prezygotic isolation mechanisms prevalent in the perch populations of Lake Constance as well. The geographical subdivision of the two populations resulting in slight differences of their peak spawning times could act to produce the early state of prezygotic isolation. This could be enhanced by mate choice decisions, leading to assortative mating  and further be promoted by postzygotic isolation based on reduced hybrid fitness as shown in this study. We showed earlier  that based on olfactory cues juvenile perch prefer their own over the other population. This indicates that a mechanism exists to differentiate between populations that could also be used to avoid mating partners of the other population. Therefore, prezygotic isolation mechanism such as population assortative mating may exist, which could be under positive selection due to reduced hybrid viability.
Since we used artificial fertilization in our laboratory experiments, we do not know whether perch will hybridize under natural conditions. So far, we have detected only slight morphological differences between the two populations (Behrmann-Godel, unpublished). Thus, it is not possible to identify parental populations and hybrids based on morphological parameters in order to survey the lake for the existence of hybrids. Genetic assignment tests will show, whether hybrids of both populations exist.
Besides indication for intrinsic postzygotic isolation, we suggest also extrinsic postzygotic isolation corroborating reproductive isolation of perch populations in Lake Constance. Each population inhabits a lake basin which is geographically connected to the other but differs in trophic state, temperature regime, mean water depth, vegetation, proportion of the littoral zone and many more biotic and abiotic parameters . Each population may be well adapted to the ecological conditions in their part of the lake; however, hybrids may experience lower fitness in either of the two parental habitats.
In conclusion we found reduced fitness in hybrids between two perch populations inhabiting Lake Constance that may have diverged rather recently, between 115 000 and 10 000 ybp. Our results provide empirical evidence for the evolution of genetic incompatibilities between the two populations that might promote reproductive isolation and drive further population divergence.
Fish sampling and artificial fertilization
Artificial fertilization was used to breed hybrids of the two perch populations of Lake Constance. In the shallower Lower Lake (western population), water temperature increases earlier in spring than in the deeper Upper Lake (eastern population) causing the western population to spawn approximately one to two weeks earlier than the eastern population. For both populations, the entire duration of spawning lasts for about one month, but most fish reproduce within one week . During peak spawning of the western population, gill nets were exposed overnight at two to three different localities (approximately 100 to 500 m apart) in both the eastern and western part of the lake (Fig. 1). Early the next morning males of the eastern population were carefully removed from the gill nets and transported alive to the western part of the lake. Females and males of the western population were removed from the gill nets and females were stripped immediately. For the hybridization experiments, egg-strands from western females were fertilized with either the sperm of a male from the western population (parental cross) or from the eastern population (hybrid cross). Six days later, egg-strands from eastern females received the same treatment, but in the reverse direction. Each fish was crossed only once. This procedure resulted in four different crosses, parental crosses from the eastern (N = 5) and western (N = 6) population, a hybrid cross F11 using females from the eastern and males from the western population (N = 7), and a hybrid cross F12 using females from the western and males from the eastern population (N = 9).
We did not initially catch sufficient numbers of ripe females from the western population to conduct all F12 hybrid crosses directly in the field. Therefore, we took seven nearly ripe western females and ripe eastern males to the laboratory. Females were kept in a 250 liter aquarium (10°C, continuous flow of lake water), males were kept in aerated water bottles. Since females may become ripe and running within a few hours, we checked the females twice a day by applying slight pressure on the abdomen. As soon as a female could be stripped (3 females on the day following capture, 3 other females during the following 5 days) the egg-strand was fertilized with the sperm of a male from the eastern population.
Breeding and acquisition of data
Fertilized egg-strands were incubated in separate tanks (9 liters, constant supply of tap water at 0.1 liter min-1, temperature 11°C, raised to 18°C during the following 4 days, 14 h of light). Three to four days after fertilization the number of eggs in each tank was reduced from several thousands to approximately 1000 by cutting out a piece of the middle part of every egg-strand. The number of unfertilized eggs was counted for each egg-strand piece. One to two days after hatching the number of hatched larvae and dead embryos was counted. These data were used to calculate the initial number of eggs per tank and find the proportion of eggs that were successfully fertilized and the proportion of larvae that successfully hatched from fertilized eggs.
To determine hybrid fitness, we used a combined fitness measure (CFM) according to Hatfield and Schluter  by multiplying the proportion of fertilized eggs by the proportion of larvae that had hatched from fertilized eggs.
We thank M. Schmid for technical assistance and A. Hodgins-Davis for improving the English. We are grateful to R. Eckmann, K. Østbye and one unknown reviewer who improved the manuscript through their constructive comments. Funding was provided by the "Deutsche Forschungsgemeinschaft" within the collaborative research center CRC 454, Littoral of Lake Constance, the "Fonds der Chemischen Industrie", the University of Konstanz, and the "Konrad Adenauer-Stiftung".
- Kawecki TJ: Sympatric speciation driven by beneficial mutations. Proc R Soc Lond B. 1996, 263: 1515-1520. 10.1098/rspb.1996.0221.View ArticleGoogle Scholar
- Turelli M, Barton NH, Coyne JA: Theory and speciation. Trend Ecol Evolut. 2001, 16: 330-343. 10.1016/S0169-5347(01)02177-2.View ArticleGoogle Scholar
- Via S: Sympatric speciation in animals: the ugly duckling grows up. Trend Ecol Evolut. 2001, 16: 381-390. 10.1016/S0169-5347(01)02188-7.View ArticleGoogle Scholar
- Porter AH, Johnson NA: Speciation despite gene flow when developmental pathways evolve. Evolution. 2002, 56 (11): 2103-2111.View ArticlePubMedGoogle Scholar
- Tregenza T, Butlin RK: Speciation without isolation. Nature. 1999, 400 (6742): 311-312. 10.1038/22419.View ArticlePubMedGoogle Scholar
- Kawecki TJ: Sympatric speciation by habitat specialization driven by deleterious mutations. Evolution. 1997, 51: 1751-1763. 10.2307/2410998.View ArticleGoogle Scholar
- Turner GF, Burrows MT: A model of sympatric speciation by sexual selection. Proc R Soc Lond B. 1995, 260: 287-292. 10.1098/rspb.1995.0093.View ArticleGoogle Scholar
- Higashi M, Takimoto G, Yamamura N: Sympatric speciation by sexual selection. Nature. 1999, 402 (6761): 523-526. 10.1038/990087.View ArticlePubMedGoogle Scholar
- Kondrashov AS, Shpak M: On the origin of species by means of assortative mating. Proc R Soc Lond B. 1998, 265: 2272-2278.View ArticleGoogle Scholar
- Dieckmann U, Doebeli M: On the origin of species by sympatric speciation. Nature. 1999, 400: 354-357. 10.1038/22521.View ArticlePubMedGoogle Scholar
- Kondrashov AS, Kondrashov FA: Interactions among quantitative traits in the course of sympatric speciation. Nature. 1999, 400 (6742): 351-354. 10.1038/22514.View ArticlePubMedGoogle Scholar
- Kirkpatrick M: Reinforcement and divergence under assortative mating. Proc R Soc Lond B. 2000, 267 (1453): 1649-1655. 10.1098/rspb.2000.1191.View ArticleGoogle Scholar
- Kirkpatrick M: Reinforcement during ecological speciation. Proc R Soc Lond B. 2001, 268 (1473): 1259-1263. 10.1098/rspb.2000.1427.View ArticleGoogle Scholar
- Doebeli M, Dieckmann U: Speciation along environmental gradients. Nature. 2003, 421: 259-264. 10.1038/nature01274.View ArticlePubMedGoogle Scholar
- Bush GL: Sympatric speciation in animals: new wine in old bottles. Trend Ecol Evolut. 1994, 9: 285-288. 10.1016/0169-5347(94)90031-0.View ArticleGoogle Scholar
- Schliewen UK, Tautz D, Paabo S: Sympatric speciation suggested by monophyly of crater lake cichlids. Nature. 1994, 368 (6472): 629-632. 10.1038/368629a0.View ArticlePubMedGoogle Scholar
- Wood CC, Foote CJ: Evidence for sympatric genetic divergence of anadromous and nonanadromous morphs of sockeye salmon (Oncorhynchus nerka). Evolution. 1996, 50 (3): 1265-1279. 10.2307/2410667.View ArticleGoogle Scholar
- Hendry AP, Wenburg JK, Paul B, Volk EC, Quinn TP: Rapid evolution of reproductive isolation in the wild: Evidence from introduced salmon. Science. 2000, 290 (5491): 516-518. 10.1126/science.290.5491.516.View ArticlePubMedGoogle Scholar
- Rolan-Alvarez E, Carballo M, Galindo J, Moran P, Fernandez B, Caballero A, Cruz R, Boulding EG, Johannesson K: Nonallopatric and parallel origin of local reproductive barriers between two snail ecotypes. Mol Ecol. 2004, 13 (11): 3415-3424. 10.1111/j.1365-294X.2004.02330.x.View ArticlePubMedGoogle Scholar
- Orr HA: The genetic basis of reproductive isolation: insights from Drosophila. Proc Natl Acad Sci USA. 2005, 102 Suppl 1: 6522-6526. 10.1073/pnas.0501893102.View ArticlePubMedGoogle Scholar
- Servedio MR, Saetre GP: Speciation as a positive feedback loop between postzygotic and prezygotic barriers to gene flow. Proc R Soc Lond B. 2003, 270 (1523): 1473-1479. 10.1098/rspb.2003.2391.View ArticleGoogle Scholar
- Rice WR, Hostert EE: Laboratory experiments on speciation: what have we learned in 40 years?. Evolution. 1993, 47: 1637-1653. 10.2307/2410209.View ArticleGoogle Scholar
- Turelli M, Orr HA: Dominance, epistasis and the genetics of postzygotic isolation. Genetics. 2000, 154 (4): 1663-1679.PubMed CentralPubMedGoogle Scholar
- Maynard Smith J: Evolutionary Genetics. 1998, New York , Oxford University Press, secondGoogle Scholar
- Payseur BA, Krenz JG, Nachman MW: Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice. Evolution. 2004, 58 (9): 2064-2078.View ArticlePubMedGoogle Scholar
- Dobzhansky T, Beadle GW: Studies on Hybrid Sterility IV. Transplanted Testes in Drosophila Pseudoobscura. Genetics. 1936, 21 (6): 832-840.PubMed CentralPubMedGoogle Scholar
- Muller HJ: Isolating mechanisms, evolution, and temperature. Biol Symp. 1942, 6: 71-125.Google Scholar
- Schluter D: Adaptive radiation in sticklebacks: trade-offs in feeding performance and growth. Ecology. 1995, 76: 82-90. 10.2307/1940633.View ArticleGoogle Scholar
- Hatfield T, Schluter D: Ecological speciation in sticklebacks: Environment-dependent hybrid fitness. Evolution. 1999, 53 (3): 866-873. 10.2307/2640726.View ArticleGoogle Scholar
- Rundle HD: A test of ecologically dependent postmating isolation between sympatric sticklebacks. Evolution. 2002, 56 (2): 322-329.View ArticlePubMedGoogle Scholar
- Bergek S, Bjorklund M: Cryptic barriers to dispersal within a lake allow genetic differentiation of Eurasian perch. Evolution. 2007, 61 (8): 2035-2041. 10.1111/j.1558-5646.2007.00163.x.View ArticlePubMedGoogle Scholar
- Heldstab H, Katoh M: Low genetic variation in perch (Perca fluviatilis L.) from three major European drainage systems in Switzerland. Aquat Sci. 1995, 57 (1): 14-18. 10.1007/BF00878023.View ArticleGoogle Scholar
- Balling TE, Pfeiffer W: Location-dependent infection of fish parasites in Lake Constance. J Fish Biol. 1997, 51 (5): 1025-1032. 10.1111/j.1095-8649.1997.tb01541.x.View ArticleGoogle Scholar
- Gerlach G, Schardt U, Eckmann R, Meyer A: Kin-structured subpopulations in Eurasian perch (Perca fluviatilis L.). Heredity. 2001, 86 (2): 213-221. 10.1046/j.1365-2540.2001.00825.x.View ArticlePubMedGoogle Scholar
- Jarv L: Migrations of the perch (Perca fluviatilis L.) in the coastal waters of western Estonia. Proceedings of the Estonian Academy of Sciences Biology Ecology. 2000, 49 (3): 270-276.Google Scholar
- Keller O, Krayss E: Die Hydrographie des Bodenseeraums in Vergangenheit und Gegenwart. Berichte der St Gallischen Naturwissenschaftlichen Gesellschaft. 2000, 89: 39-56.Google Scholar
- Behrmann-Godel J, Gerlach G, Eckmann R: Postglacial colonization shows evidence for sympatric population splitting of Eurasian perch (Perca fluviatilis L.) in Lake Constance. Mol Ecol. 2004, 13: 491-497. 10.1046/j.1365-294X.2003.02082.x.View ArticlePubMedGoogle Scholar
- Nesbø CL, Fossheim T, Vollestad LA, Jakobsen KS: Genetic divergence and phylogeographic relationships among European perch (Perca fluviatilis) populations reflect glacial refugia and postglacial colonization. Mol Ecol. 1999, 8: 1387-1404. 10.1046/j.1365-294x.1999.00699.x.View ArticlePubMedGoogle Scholar
- Orr HA, Turelli M: The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution. 2001, 55 (6): 1085-1094.View ArticlePubMedGoogle Scholar
- Coyne JA, Elwyn S, Kim SY, Llopart A: Genetic studies of two sister species in the Drosophila melanogaster subgroup, D. yakuba and D. santomea. Genet Res. 2004, 84 (1): 11-26. 10.1017/S0016672304007013.View ArticlePubMedGoogle Scholar
- Funk DJ, Nosil P, Etges WJ: Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proc Natl Acad Sci USA. 2006, 103 (9): 3209-3213. 10.1073/pnas.0508653103.PubMed CentralView ArticlePubMedGoogle Scholar
- Bolnick DI, Near TJ: Tempo of hybrid inviability in centrarchid fishes (Teleostei: Centrarchidae). Evolution. 2005, 59 (8): 1754-1767.View ArticlePubMedGoogle Scholar
- Mendelson T, Imhoff V, Iovine M: Analysis of Early Embryogenesis in Rainbow and Banded Darters (Percidae: Etheostoma) Reveals Asymmetric Postmating Barrier. Environ Biol Fish. 2006, 76 (2): 351-10.1007/s10641-006-9039-y.View ArticleGoogle Scholar
- Strathmann RR: On the barriers to hybridization between Srongylocentrotus droebachiensis (O.F. Muller) and S. pallidus (G. O. Sars). J Expl Mar Biol Ecol. 1981, 55: 39-47. 10.1016/0022-0981(81)90091-5.View ArticleGoogle Scholar
- Uehara T, Shingaki M: Studies on the fertilization and development in the two types of Echinometra mathaei from Okinawa. Zool Sci. 1984, 1: 1008-Google Scholar
- Lessios HA, Cunningham CW: Gametic incompatibility between species of the sea urchin Echinometra on the two sides of the Isthmus of Panama. Evolution. 1990, 44: 933-941. 10.2307/2409556.View ArticleGoogle Scholar
- Coyne JA, Orr HA: Patterns of speciation in Drosophila revisited. Evolution. 1989, 43: 362-381. 10.2307/2409213.View ArticleGoogle Scholar
- Tiffin P, Olson MS, Moyle LC: Asymmetrical crossing barriers in angiosperms. Proc R Soc Lond B. 2001, 268 (1469): 861-867. 10.1098/rspb.2000.1578.View ArticleGoogle Scholar
- Coyne JA: Genetics and speciation. Nature. 1992, 355: 511-515. 10.1038/355511a0.View ArticlePubMedGoogle Scholar
- Hendry AP, Day T: Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol. 2005, 14 (4): 901-916. 10.1111/j.1365-294X.2005.02480.x.View ArticlePubMedGoogle Scholar
- Russell ST: Evolution of intrinsic post-zygotic reproductive isolation in fish. Ann Zool Fennici. 2003, 40: 321-329.Google Scholar
- Price TD, Bouvier MM: The evolution of F1 postzygotic incompatibilities in birds. Evolution. 2002, 56 (10): 2083-2089.View ArticlePubMedGoogle Scholar
- Lu Q, Bernatchez L: Experimental evidence for reduced hybrid viability between dwarf and normal ecotypes of lake whitefish (Coregonus clupeaformis Mitchill). Proc R Soc Lond B. 1998, 265 (1400): 1025-1030. 10.1098/rspb.1998.0394.View ArticleGoogle Scholar
- Rogers SM, Bernatchez L: The genetic basis of intrinsic and extrinsic post-zygotic reproductive isolation jointly promoting speciation in the lake whitefish species complex (Coregonus clupeaformis). J Evolution Biol. 2006, 19 (6): 1979-1994. 10.1111/j.1420-9101.2006.01150.x.View ArticleGoogle Scholar
- Coyne JA, Orr HA: "Patterns of speciation in drosophila" revisited. Evolution. 1997, 51 (1): 295-303. 10.2307/2410984.View ArticleGoogle Scholar
- Behrmann-Godel J, Gerlach G, Eckmann R: Kin and population recognition in sympatric Lake Constance perch (Perca fluviatilis L.): can assortative shoaling drive population divergence?. Behav Ecol Sociobiol. 2006, 59: 461-468. 10.1007/s00265-005-0070-3.View ArticleGoogle Scholar
- Mürle U, Ortlepp J, Rey P: Der Bodensee: Zustand - Fakten - Perspektiven. 2004, Bregenz , Internationale Gewässerschutzkommission für den Bodensee (IGKB), 185-2Google Scholar
- Wang N, Eckmann R: Distribution of perch (Perca fluviatilis L.) during their first year of life in Lake Constance. Hydrobiologia. 1994, 277: 135-143.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.