Kravchenko, Shabanov (2008) Possible pathways of transformation of population systems

{"translated_text":"Kravchenko M. A., Shabanov D. A. Possible pathways of transformation of population systems of Pelophylax esculentus complex (Ranidae, Anura, Amphibia) // Proceedings of the Ukrainian Herpetological Society. – No. 1, 2008. – pp. 15-20.\nUDC 57.055:597.851\nPOSSIBLE PATHWAYS OF TRANSFORMATION OF POPULATION SYSTEMS OF PELOPHYLAX ESCULENTUS COMPLEX (RANIDAE, ANURA, AMPHIBIA)\nM. A. Kravchenko1, D. A. Shabanov2\nV. N. Karazin Kharkiv National University,\nSvobody Square, 4, Kharkiv, 61077 Ukraine;\nE-mail: 1m_kravchenko@inbox.ru; 2d.a.shabanov@gmail.com\nPossible pathways of transformation of population systems of Pelophylax esculentus complex (Ranidae, Anura, Amphibia). Kravchenko M. A., Shabanov D. A.— The Pelophylax esculentus complex comprises two parental species: Pelophylax lessonae (Camerano, 1882) and Pelophylax ridibundus (Pallas, 1771), as well as their hybrid — Pelophylax esculentus (Linnaeus, 1758). This group can form multicomponent population systems of various composition, which exist thanks to hemiclonal inheritance characteristic of diploid and triploid hybrid frogs. Such population systems may change over time. The paper presents a scheme of possible transformation pathways, which may serve as a basis for genealogical classification of population systems.\nKeywords: Pelophylax esculentus (Rana esculenta), hemiclonal inheritance, transformation of population systems.\nThe Central European green frog complex, Pelophylax esculentus complex, includes the pool frog (Pelophylax lessonae (Camerano, 1882), former name — Rana lessonae) and the lake frog (Pelophylax ridibundus (Pallas, 1771) = Rana ridibunda), as well as their hybrid[1] — the edible frog (Pelophylax esculentus (Linnaeus, 1758) = Rana esculenta). All three forms can inhabit the same habitats and reproduce together, forming mixed population systems (hereafter — PS). One reason for the existence of such PS is hemiclonal (clonal for individual genomes) inheritance in hybrid frogs. During gametogenesis in hybrids, one of the parental genomes may be eliminated, while the other (clonal) passes into gametes without recombination.\nPS of the P. esculentus complex are designated by capital letters of the forms that compose them (Uzzell, Berger, 1975; Lada, 1995). For example, I distinguish L‑, R‑, E‑, L‑R‑, L‑E‑, R‑E‑, and R‑E‑L‑type populations and PS. This classification does not exhaust the diversity of known green‑frog PS. Thus, some systems may include triploid individuals; in such cases, PS composed of diploid and triploid hybrids can be assigned to the Et‑type. In some PS hybrid frogs may be represented by only one sex. For instance, the R‑Em‑type PS corresponds to a mixed system of P. ridibundus and male P. esculentus (m — male), whereas the R‑Ef‑type corresponds to a similar system in which P. esculentus are represented only by females (f — female) (Lada, 1995).\nA distinctive feature of the P. esculentus complex is the high diversity of its PS even within relatively limited territories. For example, in the Kharkiv region systems of R‑, L‑, R‑E‑, R‑Et‑, R‑Em‑ and R‑E‑L‑types have been recorded (A. V. Korshunov, unpublished communication), and the existence of E‑type systems remains controversial. It should be noted that the overwhelming part of this region lies outside the range of P. lessonae, and R‑E‑type systems are generally characteristic for this area. An unexpected finding was the detection of a substantial proportion of triploids among hybrid frogs in this region (Borkin et al., 2004).\nA remarkable property of the PS of the P. esculentus complex is their capacity for transformation, which has been noted in several studies and follows from theoretical concepts about the nature of such systems (Holenweg & Reyer, 2002; Vorburger & Reyer, 2003; Mezhzheryn et al., 2005). One example of such transformations is the fate of the PS of the Ispkiv pond near the Kharkiv University biological station, examined in detail in another publication (Shabanov et al., 2006). This means that green‑frog PS should be considered not only statically but also dynamically. We proposed a possible scheme of transformation of such PS, taking into account the specifics of clonal genome transmission (Shabanov et al., 2006; A. V. Korshunov, unpublished communication). In the present work we present an expanded and refined version of this scheme (Fig. 1).\n[IMG_1]\nFig. 1. Possible pathways of transformation of population systems (PS) of Pelophylax esculentus complex.\nNotation: L — genome of Pelophylax lessonae; R — genome of Pelophylax ridibundus; L, R — non‑clonal (recombining) genomes; (L), (R) — clonal (non‑recombining) genomes.\nThe main method of this work is theoretical analysis of the literature and original data on the diversity of green‑frog population systems, taking into account concepts of hemiclonal inheritance patterns characteristic of hybrid individuals.\nA starting point for PS transformation can be considered a pure population of a parental species. Considering the possibility of colonization by frogs with different genotypes, three probable transformation pathways can be distinguished. If individuals of another parental species enter the original parental population and hybrid formation between them is impossible for any reason, the two species may coexist in the same habitat in a ratio determined by their competitive abilities under the given conditions. A return to a single‑species population is possible through competitive displacement. If hybrid individuals or individuals of another parental species that can produce hybrids enter the original PS, the fate of such PS will depend on which genomes are transmitted clonally. If the clonal genome is conspecific to the parental genome, the system will revert to its initial state in the next generation. If the clonal genome is heterospecific, the PS will begin to transform. The ratio of parental to hybrid individuals will change from generation to generation. Of the three possible crossing types in such a system, two (parent × parent and hybrid × hybrid) do not alter the proportion of main forms in the PS, whereas the third (parent × hybrid) increases the hybrid proportion. Crosses between parental and hybrid individuals with heterospecific gametes (RR × R(L) → R(L), and LL × L(R) → L(R)) produce offspring consisting only of hybrids, further increasing the hybrid share in the PS.\nThe outcome of these changes depends on several factors. The first is the survivability of the other parental species individuals that are produced by hybrid crosses, i.e., “hybridolysis” (Plotner, 2005): R(L) × R(L) → LL and L(R) × L(R) → RR. If these individuals are viable, the system shifts to the L‑E‑R‑type PS. However, individuals carrying two identical clonal genomes are often non‑viable. This effect is interpreted as a consequence of the so‑called “Müller’s ratchet” — accumulation of deleterious mutations in genomes transmitted without recombination (Hedrick, 2003).\nIf hybrid and parental viability are comparable, transformation of R‑E‑ or L‑E‑type PS may lead to complete displacement of parental forms. If hybrid offspring from hybrid × hybrid crosses are non‑viable, the PS may disappear. Nevertheless, the PS can persist in several scenarios.\nFirst, if hybrids have lower viability than parental individuals, hybrid reproductive advantage may be offset by selection favoring the parental species. The proportion of the two forms in such a PS will be governed by a balance of opposing processes.\nSecond, the appearance in a PS of hybrid individuals with heterospecific gametogenesis alongside parental forms can lead to a stable state. For PS composed of RR, R(L) and L(R) (as well as LL, L(R) and R(L)), stable ratios of the mentioned forms can exist, whereby each successive generation mirrors the previous one. Such stability may be achieved with the introduction of both diploid and, possibly, triploid hybrids. Interestingly, introduction of hybrids with conspecific gametes into a parental population causes no change. In contrast, introduction of hybrids with heterospecific gametes into a mixed parental‑hybrid system can drive the PS toward a stable state. This difference in PS response to the same stimulus reflects frequency‑independent selection.\nThird, continual immigration between local populations within the metapopulation of the P. esculentus complex can prevent PS extinction. This may give rise to migrant‑dependent PS composed of hybrids with a uniform gametogenic form. Such PS have been described for both R‑E‑ (Shabanov et al., 2006) and L‑E‑systems (Mezhzheryn et al., 2005).\nFinally, loss of parental individuals in PS that include hybrids with different gametogenesis can lead to the emergence of a “pure” E‑ or Et‑type PS (the latter when triploids are present). Colonization of the PS by particular frog forms or their loss for various reasons can provide other, not considered, transformations of the P. esculentus complex within the presented scheme.\nExamining the PS types shown in Fig. 1, we can see that they differ in the nature of their stability. The parental‑species PS is in an unstable equilibrium—it may persist for a long time, but the introduction of even a single hybrid with heterospecific gametes can trigger irreversible transformation into a transitional R‑E‑ or L‑E‑type system. The composition of the L‑R‑type PS, as well as R‑E‑ and L‑E‑types with reduced hybrid viability, reflects a balance of opposing processes. Migrant‑dependent systems with critically low reproductive numbers are in a state of degradation, whereas PS that include various hybrid forms differing in gametogenesis can be truly stable.\nIt should be emphasized that the scheme presented in Fig. 1 does not reflect the following five factors, which are crucial for PS transformation in the P. esculentus complex.\n1. Causes of the emergence of particular hybrid forms in a PS. The authors are unaware of satisfactory explanations for which parental genome becomes clonal during crosses. Existing hypotheses (greater propensity for clonal transmission of one parental genome; clonal transmission of the maternal genome, etc.) cannot account for the observed facts. The emergence of a particular hybrid form in Fig. 1 may result from parental crosses, migration of appropriate individuals from other local populations, or (hypothetically) changes in the nature of the clonal genome during hybrid reproduction.\n2. Differences between male and female clonal genomes. In frogs, the heterogametic sex is male; therefore, male clonal genomes in diploid frogs can be carried only by males, whereas female clonal genomes can be carried by both sexes. If all clonal genomes in a PS are male, one would expect hybrids to be represented only by males. The existence of PS where all hybrids are females cannot be explained by the same reason and requires a special explanation.\n3. Possibility of incomplete clonal transmission of genomes leading to recombinant individuals (Mezhzheryn et al., 2005). Crossing recombinant hybrids with parental individuals creates the possibility of gene flow across the species barrier. This mechanism, together with various forms of clonal genome evolution, should increase the diversity of clonal genomes transmitted within a PS.\n4. Existence of hybrids producing a mixture of P. lessonae and P. ridibundus gametes in a specific, individual‑specific ratio (Borkin et al., 2005).\n5. Differences between the two parental species in parameters affecting PS reproduction. The scheme in Fig. 1 is symmetric, although in the series P. lessonae — P. esculentus — P. ridibundus the average size of sexually mature individuals increases, female attractiveness rises, and male aggressiveness during mating decreases. This asymmetry leads to different dynamics of transformations and different equilibrium frequencies of frog forms in balancing and stable PS.\nFrom the authors’ perspective, the hypothetical scheme requires testing through long‑term field observations, controlled crossing and rearing experiments, as well as mathematical modelling.\nThe authors express sincere gratitude to A. I. Zinenko, A. V. Korshunov, G. A. Mazepa and S. Yu. Morozova‑Leonova for joint field research; to L. A. Atramentova, L. Ya. Borkin, G. A. Lada and S. N. Lytvynchuk for valuable criticism and discussion of results; and to M. V. Vladimirova, G. N. Zholtkevich and A. A. Lutsik for assistance in formalizing concepts of frog population systems and for mathematical modelling of their transformations.\nBorkin L. Ya., Zinenko A. I., Korshunov A. V. et al. Mass polyploidy in the hybridogenetic complex Rana esculenta (Ranidae, Anura, Amphibia) in Eastern Ukraine // Materials of the First Conference of the Ukrainian Herpetological Society. – K.: Zoological Museum of the NNP of the NAS of Ukraine, 2005. – pp. 23‑26.\nLada G. A. Central European green frogs (hybridogenetic complex Rana esculenta): introduction to the problem // Flora and Fauna of the Chernozem Region. – Tambov, 1995. – pp. 88‑109.\nMezhzheryn S. V., Morozov‑Leonova S. Yu., Nekrasova O. D. et al. Spatial structure of the hybridogenetic green‑frog complex Rana esculenta (Anura, Ranidae) in Ukraine // Materials of the First Conference of the Ukrainian Herpetological Society. – K.: Zoological Museum of the NNP of the NAS of Ukraine, 2005. – pp. 110‑144.\nHedrick F. Population Genetics. 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Phila. – 1975. – 127. – pp. 13‑24.\nVorburger C., Reyer H.-U. A genetic mechanism of species replacement in European waterfrogs? // Conservation Genetics. – 2003 – 4. – pp. 141‑155.\n\n[1] In this context the term “hybrid” denotes an evolutionary‑taxonomic unit of species rank with the scientific name Pelophylax esculentus (Dubois, 1991, 1998; see Frost, 2006) — editor’s note."}