Aquatic Ecology 32: 361–365, 1998. © 1998 Kluwer Academic Publishers. Printed in the Netherlands.
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Dwarf males in monogonont rotifers Claudia Ricci & Giulio Melone Department of Biology, State University of Milan, Via Celoria 26, 20133 Milano, Italy (Phone: +39-02-26604494; Fax: +39-02-2362726; E-mail:
[email protected]) Accepted 22 December 1998
Key words: male size, sexual dimorphism, gut vestigialization
Abstract The main characteristics of the monogonont rotifer males are haploidy, dwarfism, progenesis and gut vestigialization to varying extents. Although these traits co-occur, they are probably unlinked from the evolutionary point of view. Commonly, all of these characteristics are directly related to the small size of the male egg, equipped with a reduced amount of yolk. A more ecological approach can, however, provide additional insights. Haploidy acts as a sex determining mechanism, dwarfism and progenesis derive directly from the egg size, while gut reduction is more evident in planktonic species than in benthic ones. This discrepancy suggests that the rotifers in the two habitats are exposed to different selection pressures.
Introduction Sexual size dimorphism is exhibited by several animal groups; for instance, male vertebrates are often larger than conspecific females. This discrepancy in size is commonly the consequence of strong sexual selection (i.e., Fairbairn, 1997). Among invertebrates, the males are frequently smaller than their females, and, if they are less than 50% of female size, the males are considered to be true dwarfs. Some dwarf males, such as Bonellia, may derive their sustenance from females. This way of living was called ‘gigolism’ by Vollrath (1998). Gigolism could lead to the simplification of male body structures, and, in the extreme, the whole male could be reduced to a scrotum only, as in the anglerfish (Vollrath, 1998). Dwarfism associated with gigolism could be advantageous because several males could easily be supported by a single female who obtains, in return, more diverse sperm. In situations other than gigolism, Vollrath (1998) argued that among the driving forces that can lead to male dwarfism there may be: (1) inter-sexual negative selection, that is selection operated by females over males, like predation in spiders, or competition for food, and (2) heavy juvenile mortality of males which tend to anticipate maturation by reducing the juvenile
stage (progenesis). In addition to these, we propose that the ecological situation can affect the parental investment in offspring and lead to the production of energetically less expensive male sex. Rotifer species with dwarf males could provide valuable evidence of such a mechanism. In the phylum Rotifera, male dwarfism is known in the Monogononta class, only (Wesenberg Lund, 1923; Wallace & Snell, 1991). The sex-determining mechanism in monogonont rotifers is haplodiploidy; haploid eggs are produced through meiosis, and develop parthenogenetically into haploid males (arrenotoky); diploid eggs, either fertilized eggs or unreduced eggs produced ameiotically, develop into diploid females (Nogrady et al., 1993). Under natural conditions, monogonont males appear cyclically and occasionally. They are produced in response to very specific environmental cues and are ephemeral (Snell, 1987; Gomez & Serra, 1996). Recently, Serra and Snell (1998) suggested that the dwarf rotifer males could be the result of ‘selection on mothers to produce rapidly as many males as possible’. Here we present some considerations on the ecological importance of dwarf males in rotifers, taking into account several aspects of rotifer biology.
362 Material and methods We ran Pearson’s correlation test by matching male to female length in 54 species of monogonont rotifers, distinguishing between planktonic and benthic-littoral forms. Their ecological distribution was derived from Ruttner-Kolisko (1974) and Koste (1978). Sessile rotifers were excluded from the analysis because too little data were available in the literature. The data of both male and female sizes came from Wesenberg Lund (1923). SEM images of Brachionus plicatilis specimens during mating were obtained after induction of mixis phase on mass cultures of CCB1 clone (Valencia, Spain). Males were collected and added to young mictic females. When mating pairs were established, the animals were fixed with quick injection of OsO4 . The animals were processed for SEM observation following the protocol provided by Melone (in press).
Results and discussion Monogonont males are haploid, dwarf, progenetic and often gutless. Although these traits co-occur, they are probably unlinked from the evolutionary point of view. The traits of rotifer males may result from different selection pressures and the ecological context of the rotifers may account for their occurrence. Haploidy is probably independent of dwarfism. It acts as a sex determining mechanism and exposes the hemizygotic males to selection against the deleterious recessive mutations that may accumulate in the population during parthenogenetic reproduction (Ricci, 1992). The haploid constitution of male rotifers deeply affects their life-history traits. Size is reported to differ markedly between diploid and haploid eggs: according to Wesenberg Lund (1923), the diploid parthenogenetic egg (female-producing egg) can be twice as large, and four times as rich in yolk as the haploid parthenogenetic egg (male-producing egg). As a consequence, the male egg is energetically less expensive for the mother, who can partition the same yolk necessary for one parthenogenetic female egg into up to four male eggs. In addition, the male egg, poorer in yolk, develops faster than the female egg (Wesenberg Lund, 1923) and hatches into a smaller animal. Dwarfism: The ratio between the length of the rotifer males and their conspecific females spans from 0.15 to 1.00, but there are remarkable differences
Figure 1. Brachionus plicatilis: a dwarf male and a mictic female during copulation.
between the planktonic and benthic-littoral groups (Wesenberg Lund, 1923). Planktonic males can be regarded as true dwarfs, as the majority of species reported by Wesenberg Lund (26 out of the 34 planktonic species) are less than 50% of the length of their females. In contrast, only 4 out of the 20 benthiclittoral monogononts are true dwarfs. Small male size may have adaptive value, promoting swimming activity to contact and inseminate more females, without prohibitive increase in energy expenditures (Epp & Lewis, 1979). However, the adaptive value of the bigger benthic males has never been addressed. Each male usually fertilizes several females through hypodermic insemination (Figure 1), releasing few spermatozoa per copulation (Snell & Childress, 1987). The rotifers, eutelic and with direct development, are eutelic also for their gamete number. The sperms of the monogonont males are produced without meiosis, are scarce in number (about 30 in Brachionus plicatilis, Snell & Childress, 1987) and are already expendible at birth (Wesenberg Lund, 1923; Gilbert, 1983). Actually, the reproductive success of rotifer males is chiefly constrained by the low number of sperms that they possess, and for this reason a longer life span would not increase male fitness. A mictic female can mate with several males at different times, and even simultaneously (Figure 2) under special conditions, but the production of fertilized eggs (resting eggs) is very costly. A female can produce a few resting eggs (typically 1–2 eggs) during her lifetime (Snell & Childress, 1987). Thus, both male and sperm competition could be expected to occur in rotifer populations during the mictic periods. Progenesis produces animals ready to mate at hatching. Rotifer females have to feed to grow and reproduce, while males are already mature at birth.
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Figure 2. Brachionus plicatilis: two dwarf males copulate simultaneously the same female.
Thus, at reproduction the sex ratio (males to mictic females) of a rotifer population would be expected to be male-biased. In addition, the male-producing eggs are cheaper because they contain less yolk and develop faster than the female-producing eggs. The sexual rotifer population can be also expected to be male-biased at birth. However, there is no evidence for higher density of males from field studies (e.g. Carlin, 1943), and this could be ascribed to factors that restrict male occurrence to very short time periods. Monogonont males are produced only occasionally, sometimes once a year, and are short-lived (Snell, 1977). Thus their presence is detectable only with long-term sampling programs with frequent observations (Wesenberg Lund, 1923). In addition, the male small size can easily escape the net mesh size commonly used to sample rotifer communities. And last, but not least, rotifer males might be detected in fixed samples with some difficulty. Gut vestigialization: Many rotifer males possess a simplified or even vestigial gut, that often has no function (Wesenberg Lund, 1923), and the dwarf males live from a few hours up to a couple of days (Snell, 1977). This feature limits the use of resources by the males. The gut reduction is reported to be greater among planktonic rotifers, where male occurrence is often synchronized and male density in the population can occasionally be explosive. In contrast, the males of benthic species can have a body size as large as adult females (Wesenberg Lund, 1923). These males are expected to be able to feed in order to grow as big as their females. Actually male size, compared with female size, is particularly reduced in the rotifer species that are planktonic, and it is noticeable that, going from ben-
thos to plankton, rotifer male size seems to decrease (Figure 3). It seems that some additional selective pressure, acting on planktonic males more than on benthic males, may be expected. We could predict that benthic rotifer populations, that mostly have males capable of feeding, have a less synchronized production of males, so that their maintenance costs are diluted over time. In addition, the benthic-littoral habitat offers more composite and fragmented niches than the planktonic habitat and makes competition and predation pressures less severe. Alternatively, planktonic rotifers, exposed to heavier predation than benthic ones, avoid heavy predation by collapsing to resting stages, in analogy to copepods (Hairston et al., 1990), so that males must be produced massively for the formation of resting eggs. More field and laboratory data on predation pressures and male occurrence in the two habitats would be necessary to substantiate such hypotheses.
Conclusions Haploidy does not imply dwarfism (male bees develop from haploid eggs and are not dwarf), nor does dwarfism necessarily imply haploidy (male spiders can be dwarf, but are not haploid). The co-occurrence of dwarfism, progenesis and gut vestigialization apparently promotes male mating success: the male can move fast, is born mature, and without a gut cannot eat. Apparently rotifer male fitness is not increased by extended life, as male fertility decreases with age, but rather by increased mating opportunities, which are provided by the higher density and by the fast swimming of the males. As for the non-dwarf benthic males, they could be expected to move slower, to live longer, and possibly to hatch from more expensive eggs. Dwarfism and progenesis derive directly from the egg size, while gut reduction is likely to result into decreased food competition. Any attempt to understand the driving forces that lead to the male dwarfism should take into account the complex life cycle of the monogonont rotifers, that includes several generations of parthenogenetic females punctuated by the occasional production of males, commonly concentrated in a short time. All traits that characterize rotifer males can be directly related to the small size of the male egg that is equipped with a reduced amount of yolk. This can be interpreted as a consequence of selection on moth-
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Figure 3. The male length (µm) of planktonic ( ) and benthic-littoral (N) species of monogonont rotifers as function of the female length (µm). The regression lines and their 95% confidence bands are reported for both species groups.
ers in order to produce as many male offspring as possible in a short time, keeping reproductive costs to a minimum. This situation fits planktonic rotifer species, while benthic ones are reported to possess larger males, which either feed or hatch from bigger eggs. This discrepancy between the planktonic and benthic species suggests that the rotifers in the two habitats can be exposed to different selection pressures.
Acknowledgements Clone CCB1 of Brachionus plicatilis was kindly provided by Maria José Carmona. Ramesh Gulati, Fernando Boero and anonymous referees substantially improved this manuscript, and we gratefully acknowledge their help.
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