Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Marine Ecology. ISSN 0173-9565 REVIEW ARTICLE Latitudinal and bathymetric trends in egg size variation: a new look at Thorson’s and Rass’s rules Vladimir Laptikhovsky Falkland Islands Fisheries Department, Stanley, Falkland Islands Keywords Egg size; fish; invertebrate; larval; Rass; reproduction; reproductive strategy; Thorson. Correspondence Vladimir Laptikhovsky, Falkland Islands Fisheries Department, Stanley, FIQQ 1ZZ, Falkland Islands. E-mail: [email protected] Accepted: 5 December 2005 doi:10.1111/j.1439-0485.2006.00077.x Abstract The inverse relationship between egg size in marine animals and water temperature was simultaneously described by two outstanding marine scientists: G. Thorson and T.S. Rass. This rule consists of two different phenomena. Thorson’s rule describes ecological processes related to changes in larval biology and morphology that are caused by a selective pressure of natural selection on the different types of larval development. It belongs to the realm of macro-evolution. Rass’s rule describes physiological processes within populations and species, and between closely related species. This is not related to changes in reproductive strategy, and therefore belongs to the realm of micro-evolution and to the early stages of macro-evolution. Populations begin to produce larger eggs in colder environments because of phenotypic plasticity. Thorson’s rule describes temperature-dependent changes in the relative abundance of smalland large-egged species, whereas Rass’s rule describes a temperature-dependent relative position of both groups within an adaptive range of reproductive strategies. Problem Egg size and fecundity are very important features of a reproductive strategy and are inversely related. This is because the energy that can be invested into reproduction is restricted, leading to a trade-off between quality and quantity of offsprings (Kasyanov 1999). For this reason, differences in egg size between closely related populations, species and higher taxa could be a ‘hallmark’ of habitatdependent evolutionary patterns of reproductive strategies. Egg size is generally species-specific, although within the species it may vary within the population, e.g. with female size, food availability or spawning season. Between species, there is also an increasing trend in egg size with a decrease of temperature. This trend is called the ‘Thorson–Rass’s rule’ or ‘Thorson’s rule’ (Mileykovsky 1971) and was described simultaneously by these two scientists. Over the years it has attained a paradigm status (Levin & Bridges 2001) and is well known to all marine biologists. The expression ‘Thorson–Rass’s rule’ is more common in Russian literature, whereas ‘Thorson’s rule’ is widely recognised in the rest of the world. The third name, ‘Rass–Thorson– Marshall’s rule’ has also been proposed (Alekseev 1981) in recognition of the work of Marshall (1953) who brought data from Antarctica into the discussion. Marshall (1953) compared the results of both authors and indicated that ‘while both workers consider that selective processes have been responsible for these parallel trends, Thorson has taken into consideration biological as well as physical factors, while Rass has been more impressed with temperature condition’. Marshall (1953) also concluded that ‘… in trying to appreciate the factors which have conditioned the increase in egg size of polar and deep-sea fishes, Thorson’s (1950) approach has been followed rather than that of Rass (1941). The ecological rule proposed by Rass… is an oversimplification’. This point of view remains unchallenged to date. Marine Ecology 27 (2006) 7–14 ª 2006 The Author. Journal compilation ª 2006 Blackwell Publishing Ltd 7 Egg size variation: Thorson’s and Rass’s rules Laptikhovsky Half a century has passed since the synthetic work of Marshall (1953) was published. New data cast doubts as to whether both authors really described the same phenomenon, as commonly thought, or if there are several different ecological phenomena provoking the same ‘visible’ result? Further doubts arise from the temperaturedependent changes in egg size observed in genetic studies. The aim of this paper is to have a closer look at both rules, their implementation in natural habitats and their relation to one another. Results Thorson’s rule (changing reproductive strategy) Thorson (1936, 1946, 1950) described a trend toward increased egg size and non-planktonic, non-feeding development with increasing latitude and water depth. Both gradients involve a decrease of water temperature. Most of his work was based on gastropod molluscs from Thailand, Denmark, and Greenland, i.e. on a taxon, whose early stages of development range from pelagic larvae to that of direct development. Thorson provided a mostly ecological explanation for the phenomenon, attributing these trends to restricted food availability for planktotrophic larvae in colder waters. Later, exceptions were found in some of the most abundant species in polar seas that have feeding larvae (Pearse & Lockhart 2004). Poulin & Feral (1996) suggested that Thorson’s explanation was specific to the iceage when ice shelves when sea ice covered much more of the sea, limiting productivity, and now we probably observe its evolutionary consequences. Currently the original formulation of Thorson’s rule is replaced by one in which latitudinal and bathymetric shifts are observed in the proportions of larval planktotrophy and larval lecithotrophy (Vance 1973a,b; Levin & Bridges 2001). It assumes a generalisation to taxa which are not necessarily closely related. For example, in echinoids and bivalves, latitudinal gradients in development exist because predominantly brooding taxa dominate in the Southern Ocean (Levin & Bridges 2001). This phenomenon is almost certainly not an adaptation to low temperatures and low larval food supply, as was supposed by Thorson. Instead, the species-rich clades of brooders probably reflect enhanced speciation under unique conditions in the Antarctic that did not happen in the Arctic, where brooders are rare (Pearse & Lockhart 2004). Because Thorson’s rule involves a generalisation of data gathered from many different taxa and ecological groups, there are many exceptions to this rule (reviews: Clarke 1992; Levin & Bridges 2001; Pearse & Lockhart 2004). For example, it was found that the reproductive pattern 8 observed in marine gastropods along the Pacific coast of South America fits the predictions of Thorson’s rule very well, whereas benthic development predominates along the Atlantic coast. The scarcity of pelagic development among the Atlantic prosobranch gastropods is related to the near-continuous soft-bottom habitat and consequent prevalence of non-pelagic patterns of development that evolved (Gallardo & Penchaszadeh 2001). Reproductive strategies of most marine invertebrate taxa exist in an adaptive range from relatively highly fecund species with small eggs to relatively low-fecundity species with large eggs. Within this adaptive range of reproductive strategies, two more or less separate units of small- and large-egg species exist. This phenomenon has been shown by many authors both theoretically and empirically. The mathematical model of Vance (1973a,b) predicted that only the extremes of the range of egg size and method of nutrition (i.e. planktotrophy, lecithotrophy) were evolutionary stable. Christiansen & Fenchel (1979) presented a modified model with more realistic parameters (sigmoid larval growth and size-dependent mortality) and obtained results similar to those of Vance (1973a,b). Further advance has been made since then. For example, Roughgarden’s (1989) model included all aspects of the life cycle. This model also demonstrated that intermediate egg sizes have a disadvantage. One of the interesting results of Roughgarden’s (1989) model was that at some particular combination of growth and mortality rates, natural selection will favour the production of both smaller and larger eggs simultaneously (Havenhand 2001), i.e. contributing to a separation of one species into two with different-sized eggs. In this respect it is remarkable, particularly as most early reports of poecilogony have proved to involve cryptic or sibling species (Levin et al. 1991; Levin & Bridges 2001). The existence of sister species differing in egg size was found, for example, in octopods (Octopus bimaculatus – O. bimaculoides) (Pickford 1949) – a taxon which is very far from poecilogony. However, this phenomenon could form an important basis for the divergence in reproductive strategies and thus species evolution. Since then, much evidence of bimodal egg size distribution has been found in molluscs (Fig. 1), echinoderms and fish (Kock 1992; Winemiller & Rose 1992; Nigmatullin & Laptikhovsky 1994; Sewell & Young 1997; Laptikhovsky 1998; Jaeckle 2001; North 2001) mirroring the evolution of alternative reproductive strategies (see: Brockmann 2001). Despite the fact that there are some exceptions, it is likely that the mechanisms outlined by Vance (1973a,b) and by Christiansen & Fenchel (1979) are indeed valid (Havenhand 2001). These exceptions occur because the evolution of egg size and larval type is influenced by more factors than those considered by these Marine Ecology 27 (2006) 7–14 ª 2006 The Author. Journal compilation ª 2006 Blackwell Publishing Ltd Laptikhovsky Egg size variation: Thorson’s and Rass’s rules ronmental temperatures, but biotic factors probably play the most important role in the strategy ‘choice’. Frequency (%) 40 30 Rass’s rule (a strategy unchanged) 20 10 0 0 2 4 6 8 10 12 Egg length (mm) 14 16 28 35 Frequency (%) 30 25 20 15 10 5 0 0 4 8 12 16 20 24 28 Relative egg length (% mantle length) Fig. 1. Distribution of egg size in 82 bottom octopod species representing about a half of all known species (data from Sweeney 1992; Voss et al. 1998). authors (Havenhand 2001). Environmental patterns may diminish the occurrence of a particular reproductive style until it disappears from the habitat. For example, notothenoid fishes exhibit two reproductive strategies (small and large eggs) in the zone of seasonal pack ice presence, but are represented by only largeegged species in the proximity of Antarctic shores (Kock 1992). Both small- and large-egged groups have the same type of development although their larval biology is different (North 2001). Octopods and some fish have a direct development imitating the ecological larval stage (Boletzky 1974; Poulin et al. 2001). In the tropics and in temperate latitudes they are represented by species with both small- and large-eggs, whereas in polar regions only the large-egg species exist. These two examples also demonstrate the pressure of natural selection on the production of either small or large eggs, which can occur in ecological groups with only one extant developmental mode. Therefore, Thorson’s rule reveals itself within the adaptive range of taxon’s reproductive strategies in the past as the result of different pressure of natural selection on species with alternative developmental strategies favouring one developmental mode and suppressing another one. This leads to differences in species diversity between small- and large-egg groups, and occasionally can result in the total removal of a particular reproductive strategy from a habitat. To some extent, this phenomenon is related to envi- A similar phenomenon was described by Rass (1935, 1941, 1986), who stated it as follows: ‘‘Egg size in aquatic animals is in accordance with breeding temperatures. Among closely related species the egg size is inversely proportional to the temperatures at the moment of spawning: the eggs being larger, the nearer to the pole lies the species range’’ (Rass 1941). His results were based mostly on marine teleost fish, i.e. on a taxon with only one developmental type (in contrast to most benthic invertebrate taxa), although some data on amphibians and invertebrates were also used. Initially, he applied his discovery to closely related species (Rass 1941), but later indicated that this phenomenon could be found within species when populations from different latitudes were compared. He never extrapolated this assumption to large taxa. This phenomenon has been reported not only in marine fish, but also in fresh-water crustaceans (review: Khmelyova 1988), newts, frogs and toads (review: Rass 1986), although there are some exceptions (Lawrence & Sastry 1985; Kokita 2003). An inverse relation between egg size and temperature is also displayed by reptiles and birds but in a different altitudinal direction: from lowland plains to mountains (review: Badyaev & Ghalambor 2001). It is evident that there are no changes in developmental mode involved in this phenomenon, and as such ecological mechanisms proposed by G. Thorson and others are not applicable. Also, the trend cannot be explained by a combination of Bergmann’s rule (an increase of animal size from equator poleward) and a positive relationship between egg size and female size. Polar fish species, which produce the largest eggs, are usually much smaller in body size than their temperate relatives from the same family (Rass 1986). The phenomenon described by T.S. Rass likely has different reasons from those of Thorson’s rule, and these reasons are not precisely understood to date. Rass (1986) hypothesised that it was caused by non-proportional slowing down of the different stages of oogenesis at lower temperature that causes species-specific egg size to be larger. A temperature decrease has a similar effect on the timing of embryogenesis and provokes an increase in the species-specific number of vertebrae regardless of adult fish size. Among closely related fish species the number of vertebrae unambiguously increases poleward with egg size, not with adult size (Rass 1986). Changes in egg size, described by T.S. Rass happen in every fish family regardless of whether those representatives produce small or large eggs. Egg size increases with a decrease of temperature in Marine Ecology 27 (2006) 7–14 ª 2006 The Author. Journal compilation ª 2006 Blackwell Publishing Ltd 9 Egg size variation: Thorson’s and Rass’s rules Laptikhovsky females from the same population produce larger eggs at lower temperature. This phenomenon was briefly mentioned by Rass (1986) but not defined separately despite the fact that it is not evidently subjected to natural selection. However, both phenomena are tighly intermingled. For example, when females from three different latitudinal populations of fish, Pomacentrus coelestis, were reared in captivity at different temperatures, egg size decreased with increasing temperature in all populations (Kokita 2003). However, at each temperature egg size was always larger in the population with larger egg size in the natural habitat, demonstrating that changes in egg size were caused by interaction between both genotypic and phenotypic variation. Thus latitudinal patterns of egg-size variation may differ at the intra- and interspecific level (Kokita 2003). It is possible that this phenotypic plasticity could be partially attributed to lower demands on metabolism at lower temperature by poikilotherms, allowing them to invest more energy into individual eggs with the same genetically pre-determined fecundity. For instance, the fecundity of genetically identical (Shaw et al. 2004) autum–winter and spring–summer spawners of the squid L. gahi at the same body size is similar, but the egg size is always larger in autumn–winter spawners (Fig. 2), which reproduce at lower temperatures (Laptikhovsky et al. 2002). However, it is not a general rule, because egg size usually is inversely related to fecundity (Vance 1973a). Phenotypic plasticity in egg size was revealed in insects, particularly in Drosophila melanogaster, in which egg size Oocyte diameter (mm) A B Actual fecundity the small-egg fish family Carangidae (egg size 0.6– 1.3 mm) as well as in a large-egg genus Cateroproctus, Liparidae (egg size 4.5–9.0 mm) (Rass 1986). Latitudinal and bathymetric differences in temperatures and egg size between ranges of related species probably invoke different physiological adaptations, particularly maturation patterns such as yolk composition. Eggs of echinoderms and molluscs of the White Sea produced at lower temperatures (warm season spawning versus cold season spawning) contain more lipids in their yolk (Kaufman 1977). A relative increase of lipid content with an increase of egg size was observed not only when small eggs of planktotrophic species were compared to large eggs of lecithotrophic species, but also when compared to different-sized eggs of planktotrophic species (McEdward 1986; Jaeckle 2001). Specifically, planktotrophic eggs contained relatively more proteins than lecithotrophic eggs (40.8–59.9, mean 49.5% versus 22.2–38.4, mean 29.2%), and less lipids (19.6–23.6, mean 21.5% versus 34.5–50.3, mean 41.7%) (Jaeckle 2001). In contrast to Thorson’s rule, Rass’s rule is not related to changes in larval biology and does not assume a switch from one reproductive strategy to another, although some elements of heterochrony are possible. Yolk accumulates in greater amount at a lower temperature to such an extent occasionally that it provides nutrition not only to embryos/larvae development but also for juveniles (Lawrence & McClintock 1994). For example, eggs of the coldwater boreal loliginid squid Loligo forbesi are larger than those of relatively warm-water L. vulgaris, but the duration of embryogenesis is not sufficient to utilise all of the yolk. While L. vulgaris spends almost all of its yolk before hatching, L. forbesi goes on to use it for growth long after that (Boletzky 1987). The same was found in the sole (Baynes & Howell 1996). Another cold-water loliginid squid, Loligo gahi, whose embryogenesis is shorter than the period expected from the relation between developmental time, egg size, and temperature (Arkhipkin & Middleton 2003), also hatches with a big yolk sac, demonstrating an excess of accumulated yolk. Given this, Rass’s rule describes synchronous temperature-dependent changes in egg size in both small- and large-egg species. In colder environments, these distinctive groups shift within the adaptive range of reproductive strategies to larger eggs and lower fecundity, while the ‘ruthless’ natural selection, following Thorson’s rule, re-distributes the occurrence of these strategies within different habitats. 2.5 2.4 2.3 2.2 2.1 2 1.9 1.8 1.7 1.6 1.5 100 120 140 160 180 200 180 200 6 000 5 000 4 000 3 000 2 000 1 000 0 100 120 140 160 Mantle length (mm) Phenotypic plasticity Rass’s rule also overlaps with a third phenomenon: phenotypic plasticity in egg size. This occurs when similar-sized 10 Fig. 2. Egg size (A) and fecundity (B) in the squid Loligo gahi. Autumn–winter spawners are shown by black circles, spring–summer spawners – by empty circles. Marine Ecology 27 (2006) 7–14 ª 2006 The Author. Journal compilation ª 2006 Blackwell Publishing Ltd Laptikhovsky increases with a decrease of temperature, In this species there was also no indication of genotype–environment interaction for egg size, and evolution in egg size cannot be accounted for by differences in adult body size between populations (Azevedo et al. 1996). A similar phenomenon of plastic egg size increase at lower temperature under experimental conditions (with respective fecundity decrease) was found in a tropical butterfly Bicyclis anynana and some other arthropods (review: Steigenga et al. 2005). This trend could be disguised and even reversed by biotic factors. For example, a copepod Tortanus discaudatus produced the largest eggs in the warmest time (August), although it happens at the lowest rates of daily egg production–four times lower than in January and 12 times lower than in May (Lawrence & Sastry 1985). Therefore, this phenomenon could probably be explained by some stress-induced changes in oogenesis provoked by extremely high temperature. An increase of the cell size with a decrease of temperature is not specific to oocytes only. It was found in epidermal cells of D. melanogaster (Azevedo et al. 2002), in cells of a planarian (Romero & Baguna 1991), and in the red blood cells of a fish (Van Voorhies 1996). It is remarkable that the increase in cell size in the fruit fly occurred with no significant change in cell number, and flies reared at lower temperature were larger (Azevedo et al. 2002). Subsequently, one may suppose that the Thorson–Rass rule and the Bergmann rule are general expression of the same natural phenomenon (Van Voorhies 1996). This is generally true, because an egg (at least – a fertilised egg) and an adult animal are both literally entire organisms at a different developmental stage. Remarkably this phenotypic plasticity can be inherited, bridging a phenomenon which is of no evolutionary importance, and Rass’s rule which is subjected to a natural selection. Populations of the fruit fly, D. melanogaster that were held at 16.5 C for 9 years produced larger eggs at 25 C than populations that evolved at 25 and 29 C (Azevedo et al. 1996). A supposedly phenotypic trait became inherited! Recent investigations in insects revealed that egg size responds in a plastic manner to oviposition temperature, that egg size is heritable, and there seems to be genetic variation in the phenotypic reaction to temperature. The supposed existence of genetic variation in the temperature reaction norms challenges the widely held notion that temperature-mediated plasticity (in egg and body size) might be a purely physiological constraint (review: Steigenga et al. 2005). Discussion and conclusions The problem of latitudinal changes in egg size and reproductive modes was tackled in the middle of the 20th cen- Egg size variation: Thorson’s and Rass’s rules tury, when the two authors began to investigate it from different points of view. Thorson (1936, 1946, 1950) emphasised an importance of evolution of the different developmental styles, partially because he was working mostly on gastropods – a taxon which possesses multiple developmental modes. He attributed developmental trends to different food availability in different latitudes. Rass (1935, 1941, 1986) worked mostly on closely related fish species that possess the same developmental mode. He attributed egg size trends to temperature-dependent changes in yolk accumulation patterns. Both of them drew different conclusions because they worked on different materials and investigated different phenomena, which had the same phenotype appearance: an increase in egg size with a decrease of temperature. Another explanation was proposed by Alekseev (1981) who suggested that this increase in egg size is caused by a decrease in larval mortality with a gradual shift from complex food webs with high predator diversity in tropical seas to simpler food webs in seasonal seas and in deep waters. An extermination of eggs and larvae in tropical seas by numerous diverse predators with different hunting strategies does not allow most tropical species to adopt any other reproductive strategy but to produce as many offspring as possible and to disperse them as widely as possible. In tropical species the large eggs could be produced only in combination with extreme parental care. It was hypothesised that with a decrease of the predator diversity and simplification of the ecosystem structure in cold seas, an individual’s fitness becomes more important for survival because the competition for food becomes more intense. So, species begin to invest more energy into individual eggs (Alekseev 1981). This interesting hypothesis was published in a short abstract and was never properly investigated and described. It should also be emphasised that in a particular female the egg size could depend on food availability, body size and other internal and external factors that could change between seasons and generations (Ivankov 1985; Khmelyova 1988). It is possible to conclude that there is no single rule describing changes in egg size, but three phenomena with the same expression are under environmental influence: 1. Thorson’s rule, which acts on the macro-evolutionary level. Egg size increases with decrease of temperature, leading to changes in developmental mode and larval biology. This rule has an ecological background and is caused mostly by natural selection acting on taxa with different types of larval development. It provokes a predominance of either small- or large-egged strategists in different habitats depending on many environmental features. 2. Rass’s rule, which pertains to the micro-evolutionary level and early stages of macro-evolution. Egg size Marine Ecology 27 (2006) 7–14 ª 2006 The Author. Journal compilation ª 2006 Blackwell Publishing Ltd 11 Egg size variation: Thorson’s and Rass’s rules Laptikhovsky increases with a decrease in temperature without important changes in larval biology and morphology. This rule is likely caused by temperature-dependent changes in the species physiology. It does not change the ratio between the number of small- and large-egged species in a habitat, could apply within the same species of marine organisms, and occurs even in amphibian and terrestrial animals. 3. Phenotypic plasticity, which provokes invertebrates (not only aquatic) to produce larger eggs at lower temperature, and as in the case of Rass’s rule, is also caused by temperature-dependent changes in physiology. This appears to be an ‘extension’ of Rass’s rule. This phenomenon is not subject to natural selection unless it is inherited and becomes a subject of Rass’s rule. Both Thorson’s and Rass’s rules have different causative agents, which are still insufficiently known, and display themselves at different levels of evolution. Thorson’s rule describes the relative abundance of both small- and largeegg species. Rass’s rule describes a relative position of representatives of both these groups within the adaptive range of reproductive strategies. Processes that reveal themselves in Rass’s rule probably are a starting point, where the micro-evolution of reproductive strategies morphs into macro-evolution. Physiologically determined changes in patterns of yolk accumulation (both qualitative and quantitative) at different temperatures could be a basis first for minor changes in morphology and biology of larvae, and then in the entire developmental mode. It is difficult to say whether inheritance of acquired characters of developmental style is applicable to the temperature-dependent evolution of female gamete dimensions in poikilothermous invertebrates and vertebrates. There are quite a few examples of such inheritance of morphological features using different genetic mechanisms (reviews: Waddington 1957, 1975; Jablonka & Lamb 1995, 2005; Grodnitsky 2001, 2002; Flegr 2002; Pigliucci & Murren 2003; Lolle et al. 2005; Pigliucci 2005). They do not support a traditional understanding of Lamarckism, but they suggest that some heritable, adaptive changes come not from natural selection, but from the action of evolved internal systems that generate non-random ‘guesses’ in response to environmental changes. This would not require the abandonment of neo-darwinism, but rather its expansion beyond what Ernst Mayr contemptuously labelled ‘bean-bag genetics’ (Pigliucci 2005). Possibly, there are different mechanisms involved at the different stages of increase in egg size with decrease of temperature. First, it is an environmentally induced phenotypic plasticity that could be inherited using genomic rearrangements. Then, the temperature impact on yolk composition and accumulation patterns changes the amount of nutritional sources available for embryonic development. Eventually, it is the intensive pressure of 12 natural selection that removes all unsuccessful variations and leaves only genotypes with better fitness and reproductive performance. At low temperatures, an increasing amount of yolk makes development of a lecithotrophic strategy possible if there are no environmental constraints such as restricted opportunities for larval dispersal and settling (see: Giangrande et al. 1994; Bhaud & Duchêne 1996; Giangrande 1997; Bhaud 1998; Gallardo & Penchaszadeh 2001). The aforementioned mechanism of temperaturedependent evolution of egg size in poikilothermous marine organisms is not a final conclusion. It is rather a working hypothesis proposed for coordinated investigations of the evolution of reproductive strategies by the different methods used. Acknowledgements I would like to thank sincerely Dr. S.v. Boletzky (Lab. Arago, Banyuls sur Mer, France), Prof. Dr J.N. Havenhand (Tjärnö Mar. Biol. Lab., Göteborg, Sweden), Prof. Dr Lisa Levin (University of California, San Diego, USA), Dr K.N. Nesis (IO RAS, Moscow, Russia), Prof. Dr J. Pearse (University of California, USA), Prof. Dr S.F. Timofeev (MMBI, Murmansk, Russia), Dr P. Brickle, Dr L. Triantafillos, and Dr A. Arkhipkin (FIFD, Stanley, Falkland Islands), Dr Ch.M. Nigmatullin and Dr A.G. Arkhipov (AtlantNIRO, Kaliningrad, Russia), Dr M.R. Bhaud (Lab. Arago, Banyuls sur Mer, France), and Prof. Dr R.N. Burukovsky (KSTU, Kaliningrad, Russia) and two anonymous referees for valuable comments and consultations. References Alekseev F.E. (1981) Rass–Thorson – Marshall rule and biological structure of marine communities. In: G.G. Vinberg (Ed.), 4th Congress of All-Union Hydrobiological Society. Theses of reports. Part I. Naukova Dumka, Kiev: 4–6. Arkhipkin A.I., Middleton D.A.J. (2003) In-situ monitoring of the duration of embryonic development in the squid Loligo gahi (Cephalopoda: Loliginidae) on the Falkland shelf. Journal of Molluscan Studies, 69, 123–133. Azevedo R.B.R., French V., Partridge L. (1996) Thermal evolution of egg size in Drosophila melanogaster. Evolution, 50, 2238–2345. Azevedo R.B.R., French V., Partridge L. (2002) Temperature modulates epidermal cell sizes in Drosophila melanogaster. Journal of Insect Physiology, 48, 231–237. Badyaev A.V., Ghalambor C.K. (2001) Evolution of life histories along elevational gradients: trade-off between parental care and fecundity. Ecology, 82, 2948–2960. Baynes S.M., Howell B.R. (1996) The influence of egg size and incubation temperature on the condition of Solea solea (L.) Marine Ecology 27 (2006) 7–14 ª 2006 The Author. Journal compilation ª 2006 Blackwell Publishing Ltd Laptikhovsky larvae at hatching and first feeding. Journal of Experimental Marine Biology and Ecology, 199, 59–77. Bhaud M. (1998) The spreading potential of polychaete larvae does not predict adult distributions; consequences for conditions of recruitment. Hydrobiologia, 375/376, 35–47. Bhaud M., Duchêne J.C. (1996) Life cycle evolution: change from indirect to direct development as an adaptive answer to dissemination constraints? Oceanologica Acta, 19, 335– 346. Boletzky S.v. (1974) The ‘larvae’ of cephalopoda: a review. Thalassia Jugoslavica, 10, 45–76. Boletzky S.v. (1987) On egg capsule dimensions in Loligo forbesi (Mollusca: Cephalopoda): a note. Vie et Milieu, 37, 187–192. Brockmann H.J. (2001) The evolution of alternative strategies and tactics. Advanced Study of Behavior, 30, 1–51. Christiansen F.B., Fenchel T.M. (1979) Evolution of marine invertebrate reproductive patterns. Theoretical Population Biology, 16, 267–282. Clarke A. (1992) Reproduction in the cold: Thorson revisited. Invertebrate Reproduction and Development, 22, 175–184. Flegr J. (2002) Was Lysenko (partly) right? Michurinist biology in the view of modern plant physiology and genetics. Rivista di biologia/Biology Forum, 95, 259–272. Gallardo C.S., Penchaszadeh P.E. (2001) Hatching mode and latitude gradients in marine gastropods: revising Thorson’s paradigm in the Southern hemisphere. Marine Biology, 138, 547–552. Giangrande A. (1997) Polychaete reproductive patterns, lifecycle and life-history: an overview. Oceanography and Marine Biology: An Annual Review, 35, 323–386. Giangrande A., Geraci S., Belmonte G. (1994) Life-cycle and life-history in marine invertebrates and implications in community dynamics. Oceanography and Marine Biology: An Annual Review, 32, 305–333. Grodnitsky D.L. (2001) Epigenetic theory of evolution as a possibility of a new evolutionary synthesis. Zhurnal Obshchei Biologii, 62, 99–109 (In Russian). Grodnitsky D.L. (2002) Two Theories of Biological Evolution. Nauchnaya Knigs, Saratov (In Russian). Havenhand J.N. (2001) Evolutionary ecology of larval types. In: McEdward L. (Ed.), Ecology of Marine Invertebrate Larvae. CRC Press, London: 79–122. Ivankov V.N. (1985) Fish Fecundity: Methods of Investigation, Variability and Laws of its Formation. Edition of the Far-East University, Vladivostok (In Russian). Jablonka E., Lamb M.J. (1995) Epigenetic Inheritance and Evolution – The Lamarckian Dimension. Oxford University Press, NY, USA. Jablonka E., Lamb M.J. (2005) Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life. Bradford books, London. Jaeckle W.B. (2001) Variation in the egg size, energy content, and biochemical composition of invertebrate eggs: correlates to the mode of larval development. In: McEdward L. (Ed.), Egg size variation: Thorson’s and Rass’s rules Ecology of Marine Invertebrate Larvae. CRC Press, London: 49–77. Kasyanov V.L. (1999) Reproductive Strategy in Marine Bivalves and Echinoderms. Oxonian Press, New Delhi. Kaufman Z.S. (1977) Peculiarities of Reproductive Cycles in Invertebrates of the White Sea as Adaptation to the Existence in High Latitudes. Nauka, Leningrad (In Russian). Khmelyova N.N. (1988) Peculiarities of Crustacean Reproduction. Nauka i tekhnika, Minsk (In Russian). Kock K.H. (1992) Antarctic Fish and Fisheries. Cambridge University Press, Cambridge. Kokita T. (2003) Potential latitudinal variation in egg size and number of a geographically widespread reef fish, revealed by common-environment experiments. Marine Biology, 143, 593–601. Laptikhovsky V.V. (1998) Differentiation of reproductive strategies within a taxon, as exemplified by octopods. Ruthenica, 8, 77–80. Laptikhovsky V.V., Arkhipkin A.I., Middleton D.A.J., Butcher L.R. (2002) Ovary maturation and fecundity of the squid Loligo gahi in the southeast shelf of the Falkland Islands. Bulletin of Marine Science, 71, 449–464. Lawrence J.M., McClintock J.B. (1994) Energy acquisition and allocation by echinoderms (Echinodermata) in polar seas: adaptations for success? In: David B., Guille A., Féral J.P., Roux M. (Eds), Echinoderms Through Time. Balkema Press, Rotterdam: 39–52. Lawrence S.A., Sastry J.B. (1985) The role of temperature in seasonal variation in egg production by the copepod, Tortanus discaudatus (Thompson and Scott), in Narragansett Bay. Journal of Experimental Marine Biology and Ecology, 91, 151–167. Levin L.A., Bridges T.S. (2001) Pattern and diversity in the reproduction and development. In: McEdward L. (Ed.), Ecology of Marine Invertebrate Larvae. CRC Press, London: 2–48. Levin L.A., Zhu J., Creed E.L. (1991) The genetic basis of lifehistory characters in a polychaete exhibiting planktotrophy and lecithotrophy. Evolution, 45, 380–397. Lolle J.S., Victor J.L., Young J.M., Pruitt R.E. (2005) Genomewide non-mendelian inheritance of extra-genomic information in Arabidopsis. Nature, 3380, 505–509. Marshall N.B. (1953) Egg size in Arctic, Antarctic, and deepsea fishes. Evolution, 7, 328–341. McEdward L.R. (1986) Comparative morphometrics of echinoderm larvae. I. Some relationships between egg size and initial larval form in echinoids. Journal of Experimental Marine Biology and Ecology, 96, 251–265. Mileykovsky S.A. (1971) Types of larval development in marine bottom invertebrates, their distribution and ecological significance: a re-evaluation. Marine Biology, 10, 193–213. Nigmatullin C.M., Laptikhovsky V.V. (1994) Reproductive strategies in the squid of the family Ommastrephidae (preliminary report). Ruthenica, 4, 79–82. Marine Ecology 27 (2006) 7–14 ª 2006 The Author. Journal compilation ª 2006 Blackwell Publishing Ltd 13 Egg size variation: Thorson’s and Rass’s rules Laptikhovsky North A.W. (2001) Early life history strategies of Notothenoids at South Georgia. Journal of Fish Biology, 58, 496–505. Pearse J.S., Lockhart S.J. (2004) Reproduction in cold water: paradigm changes in the 20th century and a role for cidaroid sea urchins. Deep-Sea Research II, 51, 1533–1549. Pickford G.E. (1949) The Octopus bimaculatus problem: a study in sibling species. Bulletin Bingham Oceanography Collection, 12, 1–66. Pigliucci M. (2005) Expanding evolution: a broader view of inheritance puts pressure on the neo-darwinian synthesis. Nature, 435, 565–566. Pigliucci M., Murren C.J. (2003) Perspective: genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution, 57, 1455–1464. Poulin E., Feral J.-P. (1996) Why are so many species of brooding Antarctic echinoids? Evolution, 50, 820–830. Poulin E., Boletzky S.v., Feral J.-P. (2001) Combined ecological factors permit classification of developmental patterns in benthic marine invertebrates: a discussion note. Journal of Experimental Marine Biology and Ecology., 257, 109–115. Rass T.S. (1935) Geographische Gesetzmässigkeiten im Bau der Fischeier und Larven. Zoogeographica, 3, 90–95. Rass T.S. (1941) Geographic Parallelisms in Morphology and Development of Teleost Fish of Northern Seas. MOIP, Moscow (In Russian). Rass T.S. (1986) Biogeographic rule of inverse relation between egg size and environmental temperature in poikilothermous animals. Trudy IOAN, 116, 152–168. (In Russian). Romero R., Baguna J. (1991) Quantitative cellular analysis of growth and reproduction in fresh water planarians (Turbellaria, Tricladida). 1. A cellular description of the intact organism. Invertebrates Reproduction and Development, 19, 157–165. Roughgarden J. (1989) The evolution of marine life cycles. In: Feldmans M.W. (Ed.), Mathematical Evolutionary Theory. Princeton University Press, Princeton: 270–300. Sewell M.A., Young C.M. (1997) Are echinoderm egg size distributions bimodal? Biological Bulletin, 193, 297–305. Shaw P.W., Arkhipkin A.I., Adcock G.J., Burnett W.J., Carvalho G.R., Scherbich J.N., Villegas P.A. (2004) DNA markers 14 indicate that distinct spawning cohorts and aggregations of Patagonian squid, Loligo gahi, do not represent genetically discrete subpopulations. Marine Biology, 144, 961–970. Steigenga M.J., Zwaan B.J., Brakefield P.M., Fisher K. (2005) The evolutionary genetics of egg plasticity in a butterfly. Journal of Evolutionary Biology, 18, 281–289. Sweeney M.J. (1992) ‘‘Larval’’ and juvenile cephalopods: a manual for their identification. In: Roper C.F.E., Mangold K.M., Clarke M.R., Boletzky S.v. (Eds), Smithsonian Contribution to Zoology, Vol. 513. Smithsonian University Press, Washington, DC: 1–282. Thorson G. (1936) The larval development, growth, and metabolism of Arctic marine bottom invertebrates compared with those of other seas. Meddelingen om Grönland, 100, 1–155. Thorson G. (1946) Reproduction and larval development of Danish marine invertebrates, with special reference to the planktonic larvae in the Sound (Øresund). Meddelingen fra Komision Danmarks Fiskeri-og Havundersøgelser, 4, 1–523. Thorson G. (1950) Reproductive and larval ecology of marine invertebrates. Biological Review, 25, 1–45. Van Voorhies W.A. (1996) Bergmann size clines: a simple explanation for their occurrence in ectotherms. Evolution, 50, 1259–1264. Vance R.R. (1973a) On reproductive strategies in marine benthic invertebrates. American Naturalist, 107, 339–352. Vance R.R. (1973b) More on reproductive strategies in marine benthic invertebrates. American Naturalist., 107, 353–361. Voss N.A., Veccione M., Toll R.B., Sweeney M.J. (1998) Systematics and biogeography of cephalopods. In: Voss N.A., Veccione M., Toll R.B., Sweeny M.J. (Eds), Smithsonian Contribution to Zoology, Vol. 586. Smithsonian University Press, Washington, DC: 1–599. Waddington C.H. (1957) The Strategy of Genes: A Discussion of Some Aspects of Theoretical Biology. Allen & Unwin, London. Waddington C.H. (1975) The Evolution and Evolutionist. Edinburgh University Press, Edinburgh. Winemiller K.O., Rose K.A. (1992) Patterns of life-history diversification in North American fishes: implications for population regulation. Canadian Journal of Fisheries and Aquatic Science, 49, 2196–2218. Marine Ecology 27 (2006) 7–14 ª 2006 The Author. Journal compilation ª 2006 Blackwell Publishing Ltd