Determinants of Life-history Evolution in Nematodes

What are the determinants of parasite life-history evolution? Does life-history evolution of parasitic species differ from their free-living relatives? How and why do host and parasite life-history traits covary? Here, Serge Morand and Gabriele Sorci use recent comparative studies to investigate life-history evolution in nematodes which present both parasitic and free-living groups. Application of life-history theory to nematodes suggests that the conventional wisdom concerning the high fecundity of parasitic species could simply be the result of the larger body size of the latter when compared with free-living forms. The authors also emphasize, with the use of examples, that in most cases parasite life-history evolution depends on host features.     

Climate change and size evolution in an island rodent species: new perspectives on the island rule

As stated by the island rule, small mammals evolve toward gigantism on islands. In addition they are known to evolve faster than their mainland counterparts. Body size in island mammals may also be influenced by geographical climatic gradients or climatic change through time. We tested the relative effects of climate change and isolation on the size of the Japanese rodent Apodemus speciosus and calculated evolutionary rates of body size change since the last glacial maximum (LGM). Currently A. speciosus populations conform both to Bergmann's rule, with an increase in body size with latitude, and to the island rule, with larger body sizes on small islands. We also found that fossil representatives of A. speciosus are larger than their extant relatives. Our estimated evolutionary rates since the LGM show that body size evolution on the smaller islands has been less than half as rapid as on Honshu, the mainland-type large island of Japan. We conclude that island populations exhibit larger body sizes today not because they have evolved toward gigantism, but because their evolution toward a smaller size, due to climate warming since the LGM, has been decelerated by the island effect. These combined results suggest that evolution in Quaternary island small mammals may not have been as fast as expected by the island effect because of the counteracting effect of climate change during this period.     

How host size may constrain the evolution of parasite body size and clutch size. The parasitic isopod Ichthyoxenus fushanensis and its host fish, Varicorhinus bacbatulus, as an example

The flesh-burrowing parasitic isopod Ichthyoxenus fushanensis was found infecting the body cavity of a freshwater fish, Varicorhinus bacbatulus , in heterosexual pairs. Herein we investigate the question of how the host body size may constrain the parasite size and clutch size by analyzing the interactions among the body size and clutch size of the parasite, and host size. Due to the low transmission rate of I. fushanensis to its host and the positive relationship between clutch size and female size, selection may favor larger females with larger clutch sizes to compensate for massive losses of manca (the free-living juveniles). The path model reveals that clutch size depends not only directly on female size, but also on the sizes of her host and mate. Female size also depends on the sizes of the host and her mate. A negative correlation exists between the body sizes of the paired males and females. This negative correlation may be regarded as a consequence of competition for limited available space or other resources provided by the host. The effects of host size on parasite size, however, act on the total volume of both sexes as a whole, not specifically on either the female or the male. In this case, the available space/resources may not allow both individuals of different sexes to evolve toward a larger size simultaneously. Under the constraint of host size, a strategy of reducing the body size of the paired male may provide a way to increase the body size of the paired female and achieve a larger clutch size.     

CLUTCH SIZE AND EGG SIZE IN FREE-LIVING AND PARASITIC COPEPODS: A COMPARATIVE ANALYSIS

The evolution of reproductive strategies and the trade-off between number and size of eggs were investigated in a comparative analysis of free-living and parasitic copepods. Data from 1038 copepod species were used to obtain family averages for 105 families; the phylogenetic relationships among these families include 94 branching events or 94 independent contrasts on which the analysis was based. Transition from a free-living existence to parasitism on invertebrates resulted in small increases in body size. Transition from parasitism on invertebrates to parasitism on fish was associated with greater increases in body size. After controlling for body size, a switch to fish hosts resulted in an increase in the number of eggs produced and a reduction in egg size. Among all contrasts, there was a negative relationship between changes in relative clutch size and changes in relative egg size, suggesting the existence of a trade-off between egg size and numbers. However, opposite changes in these measures of clutch size and egg size were not quite more frequent than expected by chance, therefore indicating that investments into egg numbers are not necessarily made at the expense of egg size, and vice versa. Latitude affected copepod body size, clutch size, and egg size, whereas the effects of freshwater colonization or size of the fish host were not significant. Comparative analyses at either the genus or species levels within given taxa of copepods parasitic on fish provided limited support for a trade-off between clutch size and egg size, but were hampered by the small number of independent phylogenetic contrasts available. From the family-level comparative analysis, it appears that the evolutionary transition from a free life to parasitism on invertebrates, and the transition from parasitism on invertebrates to parasitism on fish, have led to changes in life-history traits in response to the different selective pressures associated with the different modes of life.     

Evolution and ecology of lizard body sizes

Aim Body size is instrumental in influencing animal physiology, morphology, ecology and evolution, as well as extinction risk. I examine several hypotheses regarding the influence of body size on lizard evolution and extinction risk, assessing whether body size influences, or is influenced by, species richness, herbivory, island dwelling and extinction risk. Location World‐wide. Methods I used literature data and measurements of museum and live specimens to estimate lizard body size distributions. Results I obtained body size data for 99% of the world's lizard species. The body size–frequency distribution is highly modal and right skewed and similar distributions characterize most lizard families and lizard assemblages across biogeographical realms. There is a strong negative correlation between mean body size within families and species richness. Herbivorous lizards are larger than omnivorous and carnivorous ones, and aquatic lizards are larger than non‐aquatic species. Diurnal activity is associated with small body size. Insular lizards tend towards both extremes of the size spectrum. Extinction risk increases with body size of species for which risk has been assessed. Main conclusions Small size seems to promote fast diversification of disparate body plans. The absence of mammalian predators allows insular lizards to attain larger body sizes by means of release from predation and allows them to evolve into the top predator niche. Island living also promotes a high frequency of herbivory, which is also associated with large size. Aquatic and nocturnal lizards probably evolve large size because of thermal constraints. The association between large size and high extinction risk, however, probably reflects a bias in the species in which risk has been studied.     

Increased body size confers greater fitness at lower experimental temperature in male Drosophila melanogaster

Genetic variation of body size along latitudinal clines is found globally in Drosophila melanogaster, with larger individuals encountered at higher latitudes. Temperature has been implicated as a selective agent for these clines, because the body size of laboratory populations allowed to evolve in culture at lower temperatures is larger. In this study, we investigated the hypothesis that larger size is favoured at lower temperature through natural selection on adult males. We measured life‐span and age‐specific fertility of males from lines of flies artificially selected for body size at two different experimental temperatures. There was an interaction between experimental temperature and body size selection for male fitness; large‐line males were fitter than controls at both temperatures, but the difference in fitness was greater at the lower experimental temperature. Smaller males did not perform significantly differently from control males at either experimental temperature. The results imply that thermal selection for larger adult males is at least in part responsible for the evolution of larger body size at lower temperatures in this species. The responsible mechanisms require further investigation.     

The evolution of life-history traits in parasitic and free-living platyhelminthes: a new perspective

Parasite life histories have been assumed to be shaped by their particular mode of existence. To test this hypothesis, we investigate the relationships between life-history traits of free-living and parasitic platyhelminthes. Using phylogenetically independent contrasts we examine patterns of interspecific covariation in adult size, progeny volume, daily fecundity, total reproductive capacity, age at first reproduction and longevity. The correlations obtained indicate a similar causal chain of life history variations for free-living and parasitic platyhelminthes. These results suggest that increased longevity favours delayed reproduction. Furthermore, growth pattern determines adult body size and age at maturity. For platyhelminthes, whether free-living or parasitic, the total reproductive capacity is found to be directly determined by the size of the worm. Within this group the parasitic way of life does not seem to influence the basic patterns of life history evolution. Received: 20 September 1997 / Accepted: 1 March 1998     

Correlated evolution of conspicuous coloration and body size in poison frogs (Dendrobatidae)

Conspicuous coloration is often used in combination with chemical defenses to deter predators from attacking. Experimental studies have shown that the avoidance inducing effect of conspicuous prey coloration increases with increasing size of pattern elements and with increasing body size. Here we use a comparative approach to test the prediction from these findings, namely that conspicuous coloration will evolve in tandem with body size. In our analysis, we use a previously published mitochondrial DNA-based phylogeny and comparative analysis of independent contrasts to examine if evolutionary shifts in color pattern have been associated with evolutionary changes in body size in aposematic poison frogs (Anura: Dendrobatidae). Information on body size (snout to vent length) and coloration were obtained from the literature. Two different measures of conspicuousness were used, one based on rankings by human observers and the other based on computer analysis of digitized photographs. The results from comparative analyses using either measure of coloration indicated that avoidance inducing coloration and body size have evolved in concert in poison frogs. Results from reconstruction of character change further indicate that the correlated evolution of size and coloration has involved changes in both directions within each of the different clades of the phylogenetic tree. This finding is consistent with the hypothesis that selection imposed by visually guided predators has promoted the evolution of larger body size in species with conspicuous coloration, or enhanced evolution of conspicuous coloration in larger species.     

Ecological specialization in fossil mammals explains Cope's rule

Cope's rule is the trend toward increasing body size in a lineage over geological time. The rule has been explained either as passive diffusion away from a small initial body size or as an active trend upheld by the ecological and evolutionary advantages that large body size confers. An explicit and phylogenetically informed analysis of body size evolution in Cenozoic mammals shows that body size increases significantly in most inclusive clades. This increase occurs through temporal substitution of incumbent species by larger-sized close relatives within the clades. These late-appearing species have smaller spatial and temporal ranges and are rarer than the incumbents they replace, traits that are typical of ecological specialists. Cope's rule, accordingly, appears to derive mainly from increasing ecological specialization and clade-level niche expansion rather than from active selection for larger size. However, overlain on a net trend toward average size increase, significant pulses in origination of large-sized species are concentrated in periods of global cooling. These pulses plausibly record direct selection for larger body size according to Bergmann's rule, which thus appears to be independent of but concomitant with Cope's.     

Body size evolution of oxyurid (Nematoda) parasites: the role of hosts

Studying the diversification of body size in a taxon of parasites allows comparison of patterns of variation observed in the parasites with patterns found in free-living organisms. The distributions of body size of oxyurid nematodes (obligate parasites of vertebrates and invertebrates) are lognormally right-skewed, except for male oxyurids in invertebrates which show left-skewed distributions. In these parasitic forms, speciose genera do not have the smallest body sizes. Parasite body size is positively correlated with host body size, the largest hosts possessing the largest parasites. This trend is shown to occur within one monophyletic group of oxyurids, those of Old World primates. Comparative methods are used to take account of the effects of phylogeny. The use of multiple linear regression on distance matrices allows measurements of the contribution of phylogeny to the evolution of body size of parasites. Evolution of body size in female pinworms of Old World primates appears to be dependent only on the body size of their hosts. The tendency of parasite body size to increase with host body size is discussed in the light of the evolution of life-history traits.     

Cytological paradoxes in the developmental cycle of the coelenterate Polypodium hydriforme--an intracellular parasite from the oocytes of acipenserid fishes

Successive stages of the embryonic development of Polypodium hydriforme, occurring at the parasitic phase of its life cycle, are considered. The development of a new parasitic generation starts without fertilization, i. e. parthenogenetically. The embryo develops from aberrant binucleate gametes formed in the result of meiosis within entodermal gonads of free-living animals. This type of gametogenesis, earlier considered as spermatogenesis (Raikova, 1961), is now interpreted as oogenesis. A conclusion is drawn about a change of the sexual orientation of the male gonad which becomes a female one in the course of evolution of Polypodium. As to the gonads of free-living animals, which were formerly interpreted as female ones, they seem to be abortive rudimentary organs since they produce no mature sex cells. A long-lasting block of cytokinesis of the 2nd meiotic division, as well as utilization of the polar body of this division as a phorocyte and, later, as a trophamnion, are important adaptations of Polypodium to parasitism. It is the larger nucleus with a voluminous cytoplasm, rather than the smaller nucleus, that becomes here the 2nd polar body. Polypodium differs from other coelenterates by the presence of highly polyploid feeding cells at both the parasitic (the trophamnion, 500 c) and free-living phases of the life cycle (trophocytes in the rudimentary female gonad, 8c-32c).     

Evolutionary branching under asymmetric competition

I investigate the evolution of a continuous trait, such as body size or arms level, which affects the outcome of competitive contests such that the contestant with the larger trait value has a higher probability of winning. I show that a polymorphism of distinctly different strategies can evolve in an initially monomorphic population even if mutations have only small phenotypic effect. In a simple Lotka-Volterra-type model of asymmetric competition, I derive the conditions under which two strategies can gradually evolve from a single ancestral strategy; the evolution of higher level polymorphisms is studied by numerical analysis and computer simulations of specific examples. High levels of polymorphism may build up during evolution. The coevolution of strategies in polymorphic populations, however, may also lead to extinction, which decreases the level of polymorphism. I discuss whether the evolution of several haploid strategies from a single initial strategy may correspond to the evolution of several sympatric species in a diploid outbreeding population.     

The island rule: made to be broken?

The island rule is a hypothesis whereby small mammals evolve larger size on islands while large insular mammals dwarf. The rule is believed to emanate from small mammals growing larger to control more resources and enhance metabolic efficiency, while large mammals evolve smaller size to reduce resource requirements and increase reproductive output. We show that there is no evidence for the existence of the island rule when phylogenetic comparative methods are applied to a large, high-quality dataset. Rather, there are just a few clade-specific patterns: carnivores; heteromyid rodents; and artiodactyls typically evolve smaller size on islands whereas murid rodents usually grow larger. The island rule is probably an artefact of comparing distantly related groups showing clade-specific responses to insularity. Instead of a rule, size evolution on islands is likely to be governed by the biotic and abiotic characteristics of different islands, the biology of the species in question and contingency.     

CHAOBORUS PREDATION AND LIFE-HISTORY EVOLUTION IN DAPHNIA PULEX: TEMPORAL PATTERN OF POPULATION DIVERSITY,FITNESS, AND MEAN LIFE HISTORY

The effect of predation by the aquatic dipteran larva Chaoborus americanus on genetic diversity and life-history evolution in the cladoceran Daphnia pulex was investigated in large replicate laboratory populations. Instantaneous daily loss rates of clonal diversity and genetic variance for fitness indicate that 93–99% of initial genetic diversity can be removed from populations during the 8–12 generations of clonal reproduction that occur each year in natural populations. In the absence of predation, the principal evolved changes in mean population life history were smaller immature body size and increased and earlier fecundity. In the presence of size-selective Chaoborus predation, populations evolved toward larger body size and increased and earlier reproduction. The difference between these two trajectories is an estimate of the direct additive effect of Chaoborus predation. This effect was manifested as evolution toward larger body size with a trend toward earlier and increased reproduction.     

Individual-level selection as a cause of Cope's rule of phyletic size increase

Cope's rule, the tendency for species within a lineage to evolve towards larger body size, has been widely reported in the fossil record, but the mechanisms leading to such phyletic size increase remain unclear. Here we show that selection acting on individual organisms generally favors larger body size. We performed an analysis of the strength of directional selection on size compared with other quantitative traits by evaluating 854 selection estimates from 42 studies of contemporaneous natural populations. For size, more than 79% of selection estimates exceed zero, whereas for other morphological traits positive and negative values are similar in frequency. The selective advantage of increased size occurs for traits implicated in both natural selection (e.g., differences in survival) and sexual selection (e.g., differences in mating success). The predominance of positive directional selection on size within populations could translate into a macroevolutionary trend toward increased size and thereby explain Cope's rule.     

Single and multigenerational responses of body mass to atmospheric oxygen concentrations in Drosophila melanogaster : evidence for roles of plasticity and evolution

Greater oxygen availability has been hypothesized to be important in allowing the evolution of larger invertebrates during the Earth’s history, and across aquatic environments. We tested for evolutionary and developmental responses of adult body size of Drosophila melanogaster to hypoxia and hyperoxia. Individually reared flies were smaller in hypoxia, but hyperoxia had no effect. In each of three oxygen treatments (hypoxia, normoxia or hyperoxia) we reared three replicate lines of flies for seven generations, followed by four generations in normoxia. In hypoxia, responses were due primarily to developmental plasticity, as average body size fell in one generation and returned to control values after one to two generations of normoxia. In hyperoxia, flies evolved larger body sizes. Maximal fly mass was reached during the first generation of return from hyperoxia to normoxia. Our results suggest that higher oxygen levels could cause invertebrate species to evolve larger average sizes, rather than simply permitting evolution of giant species.     

Parasitic castration of a vertebrate: Effect of the cymothoid isopod, Anilocra apogonae, on the five-lined cardinalfish, Cheilodipterus quinquelineatus

Parasitic castration, the specific blocking of host reproductive output by an individual parasite, is a host-parasite interaction common to many invertebrates, particularly crustaceans, echinoderms and molluscs. It can reduce host density, alter host population dynamics and the evolution of host life history traits. Here we show that parasitisation by a single female cymothoid isopod, Anilocra apogonae, castrates its vertebrate host, the five-lined cardinalfish, Cheilodipterus quinquelineatus. Parasitised male fish fail to mouthbrood their young. The gonads of parasitised fish are smaller and parasitised female fish have substantially fewer and smaller ova than do the gonads of unparasitised fish. As for parasitic castrators of invertebrate hosts, A. apogonae on C. quinquelineatus are uniformly dispersed amongst infested hosts (one adult female isopod per host), are site specific, and their body size is highly correlated with that of their host. These isopods are large relative to the body size of their hosts, averaging 3.8% of the weight of the host. Parasitised fish also weigh less and are shorter than unparasitised fish of the same age. Despite the presence of other potential hosts, A. apogonae only infests C. quinquelineatus. The consistency of the ecological correlates amongst known parasitic castrators suggests that the parasitic castrator host-parasite relationship will be recognised for other parasites of vertebrates.     

Evolutionary causes of male-biased sexual size dimorphism from a female perspective in the seed bug Togo hemipterus (Heteroptera: Lygaeidae)

Sexual size dimorphisms (SSDs) in body size are expected to evolve when selection on female and male sizes favors different optima. Many insects show female-biased SSD that is usually explained by the strong fecundity advantage of larger females. However, in some insects, males are as large as or even larger than females. The seed bug Togo hemipterus (Scott) also exhibits a male-biased SSD in body size. Many studies that have clarified the evolutionary causes of male-biased SSD have focused only on male advantages due to male–male competition. To clarify the evolutionary causes of male-biased SSD in body size, we should examine the degree of not only the sexual selection that favors larger males but also natural selection that is acting on female fecundity. The obtained results, which showed higher mating acceptance rates to larger males, implies that females prefer larger males. No significant relationship was detected between female body size and fecundity; body size effects on female fecundity were weak or undetectable. We conclude that male-biased SSD in T. hemipterus can be accounted for by a combination of sexual selection through male–male competition and female choice favoring large males, plus weak or undetectable natural selection that favors large females due to a fecundity advantage.     

Conspicuous visual signals do not coevolve with increased body size in marine sea slugs

Many taxa use conspicuous colouration to attract mates, signal chemical defences (aposematism) or for thermoregulation. Conspicuousness is a key feature of aposematic signals, and experimental evidence suggests that predators avoid conspicuous prey more readily when they exhibit larger body size and/or pattern elements. Aposematic prey species may therefore evolve a larger body size due to predatory selection pressures, or alternatively, larger prey species may be more likely to evolve aposematic colouration. Therefore, a positive correlation between conspicuousness and body size should exist. Here, we investigated whether there was a phylogenetic correlation between the conspicuousness of animal patterns and body size using an intriguing, understudied model system to examine questions on the evolution of animal signals, namely nudibranchs (opisthobranch molluscs). We also used new ways to compare animal patterns quantitatively with their background habitat in terms of intensity variance and spatial frequency power spectra. In studies of aposematism, conspicuousness is usually quantified using the spectral contrast of animal colour patches against its background; however, other components of visual signals, such as pattern, luminance and spectral sensitivities of potential observers, are largely ignored. Contrary to our prediction, we found that the conspicuousness of body patterns in over 70 nudibranch species decreased as body size increased, indicating that crypsis was not limited to a smaller body size. Therefore, alternative selective pressures on body size and development of colour patterns, other than those inflicted by visual hunting predators, may act more strongly on the evolution of aposematism in nudibranch molluscs.     

The Role of Sex-specific Plasticity in Shaping Sexual Dimorphism in a Long-lived Vertebrate,the Snapping Turtle <Emphasis Type="Italic">Chelydra serpentina</Emphasis>

Sex-specific plasticity, the differential response that the genome of males and females may have to different environments, is a mechanism that can affect the degree of sexual dimorphism. Two adaptive hypotheses have been proposed to explain how sex-specific plasticity affects the evolution of sexual size dimorphism. The adaptive canalization hypothesis states that the larger sex exhibits lesser plasticity compared to the smaller sex due to strong directional selection for a large body size, which penalizes individuals attaining sub-optimal body sizes. The condition-dependence hypothesis states that the larger sex exhibits greater plasticity than the smaller sex due to strong directional selection for a large body size favoring a greater sensitivity as an opportunistic mechanism for growth enhancement under favorable conditions. While the relationship between sex-specific plasticity and sexual dimorphism has been studied mainly in invertebrates, its role in long-lived vertebrates has received little attention. In this study we tested the predictions derived from these two hypotheses by comparing the plastic responses of body size and shape of males and females of the snapping turtle (Chelydra serpentina) raised under common garden conditions. Body size was plastic, sexually dimorphic, and the plasticity was also sex-specific, with males exhibiting greater body size plasticity relative to females. Because snapping turtle males are larger than females, sexual size dimorphism in this species appears to be driven by an increased plasticity of the larger sex over the smaller sex as predicted by the condition-dependent hypothesis. However, male body size was enhanced under relatively limited resources, in contrast to expectations from this model. Body shape was also plastic and sexually dimorphic, however no sex by environment interaction was found in this case. Instead, plasticity of sexual shape dimorphism seems to evolve in parallel for males and females as both sexes responded similarly to different environments.