Evolution of Intrinsic Post-Zygotic Reproductive Isolation in Fish

Ann. Zool. Fennici 40: 321–329 ISSN 0003-455X Helsinki 29 August 2003 © Finnish Zoological and Botanical Publishing Board 2003 Evolution of intrinsic post-zygotic reproductive isolation in fi sh Stephen T. Russell Gatty Marine Laboratory, School of Biology, University of St. Andrews, St. Andrews, Scotland, KY16 8LB (e-mail: [email protected]) Received 5 Feb. 2003, revised version received 3 June 2003, accepted 4 June 2003 Russell, S. T. 2003: Evolution of intrinsic post-zygotic reproductive isolation in fi sh. — Ann. Zool. Fennici 40: 321–329. The comparative approach is important in investigating the evolution of reproductive isolation. Yet this method has not been extended to teleost fi sh, the most diverse vertebrate lineage. Many experimental interspecifi c crosses have been performed in aquacultural research, and some of the resultant data is analysed in relation to mitochondrial cytochrome b divergence to investigate the evolution of intrinsic postzygotic isolation. Such isolation was found to increase gradually, suggesting that hybrid unfi tness is usually due to the gradual accumulation of deleterious epistatic interactions among species. Hybrid sterility evolved more rapidly than inviability, although both forms of hybrid fi tness are probably important in isolating natural populations. Because of general diffi culties in characterising fi sh genetic sex-determination systems, and because of the plethora of systems potentially represented in any given cross, too few crosses are currently available to evaluate the generality of Haldaneʼs rule in fi sh. Introduction emerge from these analyses. Hybrid sterility tends to evolve sooner than hybrid inviability Speciation is a typically slow process whose in taxa as divergent as Lepidoptera (Presgraves genetical basis requires substantial effort to elu- 2002), Drosophila (Coyne & Orr 1989, 1997) cidate. Furthermore, taxa differ in their modes and birds (Price & Bouvier 2002). This is prob- and rates of speciation (Mayr 1942). Thus, com- ably because sex- and reproduction-related parative approaches are an important means of genes evolve more rapidly than viability-related identifying general phenomena characterising ones (Singh & Kulathinal 2000). Also evident speciation (e.g., Coyne & Orr 1989, 1997), and is Haldaneʼs rule: “when, in the F1 offspring of potentially of discerning the relative importance two different animal races, one sex is absent, of different speciation mechanisms (e.g., Pres- rare, or sterile, that sex is the heterozygous [het- graves 2002). erogametic] sex (Haldane 1922).” Haldaneʼs rule Comparative analyses considering the evo- is very widespread and has been documented lution of intrinsic post-zygotic reproductive in both groups with heterogametic males (e.g., isolation (RI) relate the magnitude of RI (as Mammalia, Amphibia, Reptilia), and those with assayed by hybrid sterility and inviability) to heterogametic females (Diptera, Orthoptera, genetic divergence. Several notable patterns Heteroptera, Lepidoptera, birds) (Coyne & Orr 322 Russell • ANN. ZOOL. FENNICI Vol. 40 1989, 1997, Laurie 1997, Orr 1997, Presgraves trends are apparent in the development of intrin- 2002, Price & Bouvier 2002). Haldaneʼs rule is sic post-zygotic RI. Equivalent data for sexual probably a composite phenomenon refl ecting isolation are relatively lacking, so this isolation both faster male evolution (through sexual selec- mechanism is not considered here. tion) and the recessivity of x-linked genes gen- erating hybrid unfi tness (the Dominance theory) (Laurie 1997, Orr 1997). Material and methods Various mechanisms can induce intrinsic post-zygotic RI; for example, founder-effect spe- Data on hybrid unfi tness were obtained from ciation (Carson & Templeton 1984), differences interspecifi c crosses largely described in Argue in ploidy between related taxa (Stebbins 1950), and Dunham (1999) and Ryabov (1981) (see and microbe-induced isolation (Werren 1998). Appendix). Consideration was limited to F1 However, the Dobzhansky-Muller model has the viability and fertility as in equivalent compara- greatest general explanatory power. Dobzhansky tive studies of other organisms. Thus, although (1936) and Muller (1940) considered that hybrid many studies have documented gross hybrid sterility and inviability result as pleiotropic by- breakdown only in later hybrid generations products of independent evolution in allopatric (Edmands 2002), due to break-up of parental populations. In the Dobzhansky-Muller (D-M) gene combinations through recombination, model, alleles that enhance fi tness on the normal these were discarded. Analysis was limited to genetic background may lower fi tness when studies that had examined fertility and viability brought together in hybrids with alleles from of both sexes. Asymmetries in the strength of another taxa. Thus, RI results from the accu- post-zygotic RI between reciprocal crosses often mulation of deleterious epistatic interactions exist (e.g., Tiffi n et al. 2001). However, recipro- in hybrids. Empirical and theoretical studies cal crosses were usually not distinguished in implicate natural selection in the accumulation of the source literature, so they are generally not D-M incompatibilities (e.g., Coyne et al. 1997, distinguished here; in the occasional instances Turelli et al. 2001). Theoretical analyses indicate when reciprocal cross data was available, crosses that D-M incompatibilities are rare and that the were averaged across. Similarly, different races severity of hybrid unfi tness and the number of of a particular species can be isolated to differing loci underlying incompatibilities should increase degrees with the same taxon (Argue & Dunham as the square of time separating two taxa (Orr 1999); although any such instances identifi ed in 1995, Orr & Turelli 2001). So, the D-M model the literature happened to be discarded from this predicts an approximately regular rate in the analysis because of phylogenetic non-independ- acquisition of RI, in contrast to other post- ence, this caveat remains potentially important. zygotic RI mechanisms that typically induce The magnitude of RI was coded from 0 (both speciation instantaneously (e.g., founder-effect sexes viable and fertile) to 4 (both sexes invi- speciation, ploidy differences, etc.). Compara- able). A code of “2” means that both sexes are tive studies may therefore be used to evaluate viable but sterile, such that effectively complete the relative importance of different isolation intrinsic RI exists (see Fig. 1 for isolation index mechanisms. classifi cation). Fish are the most diverse vertebrate lineage, Mitochondrial cytochrome b sequences were yet RI evolution in fi sh has not been considered obtained from GenBank (accession numbers are within a comparative context. Many experimen- given in the Appendix) and aligned using Clus- tal crosses have involved teleost fi sh taxa for talX (Thompson et al. 1994). Pairwise distance aquacultural research (for example, Schwartz estimates were estimated using the Kimura-2- (1981) lists over 1800 studies), and these con- parameter implemented in Mega v. 2.0 (Kumar stitute a large and important, but unexploited et al. 2001). The cytochrome-b gene, unlike resource. Here, I examine a small subset of these allozymes, is unlikely to be affected by selection crosses in relation to mitochondrial cytochrome on traits conferring RI (Fitzpatrick 2002), and is b divergence, and investigate whether general therefore an appropriate basis for genetic dis- ANN. ZOOL. FENNICI Vol. 40 • Evolution of post-zygotic isolation in fi sh 323 family corrected tance estimation. However, mitochondrial DNA 4 exhibits rate variation between different lineages non-family corrected (Rand 1994), and is generally only useful for lin- 3 eages separated by < 10 myr because of satura- tion properties (Meyer 1994). These caveats are 2 considered further in the Discussion. A further 1 caveat that may be only occasionally important Post-zygotic isolation index is that interspecifi c introgessive hybridisation 0 05 1015202530 involving mitochondrial DNA may lead to under- Cytochrome b sequence divergence (%) estimation of overall genetic divergence (Smith 1992). Fig. 1. Plot of intrinsic post-zygotic reproductive isola- In ensuring phylogenetic independence of the tion against mitochondrial cytochrome b distances (Kimura-2-parameter corrected). Isolation index is as cross data crosses were not averaged across (e.g., follows: 0, both sexes fertile; 0.5, one sex fertile, the by following Felsensteinʼs (1985) phylogeneti- other sex some individuals recorded as fertile; 1, one cally independent contrasts method) because of sex fertile, one sex viable but infertile; 1.5, one sex current uncertainties in phylogenetic relation- sometimes fertile, one sex viable but infertile; 2, both ships amongst higher-order taxa. Instead, two sexes viable but infertile; 2.5, one sex viable but infertile, one sex sometimes viable; 3, one sex viable, one alternative approaches were adopted: (1) follow- sex missing; 3.5, one sex sometimes viable, one sex ing Price and Bouvier (2002), a list of crosses missing; 4, both sexes missing. All data derives from was prepared wherein each species was repre- method 1 for controlling phylogenetic dependence, sented in only one cross; (2) in a more robust wherein species were only considered in one cross, analysis based on the database generated by (1), irrespective of familial membership. The family-corrected subclass considers only one cross per family only one cross per

Load more