Evolution of body size in Galapagos marine iguanas

Body size is one of the most important traits of organisms and allows predictions of an individual's morphology, physiology, behaviour and life history. However, explaining the evolution of complex traits such as body size is difficult because a plethora of other traits influence body size. Here I review what we know about the evolution of body size in a group of island reptiles and try to generalize about the mechanisms that shape body size. Galapagos marine iguanas occupy all 13 larger islands in this Pacific archipelago and have maximum island body weights between 900 and 12 000g. The distribution of body sizes does not match mitochondrial clades, indicating that body size evolves independently of genetic relatedness. Marine iguanas lack intra- and inter-specific food competition and predators are not size-specific, discounting these factors as selective agents influencing body size. Instead I hypothesize that body size reflects the trade-offs between sexual and natural selection. We found that sexual selection continuously favours larger body sizes. Large males establish display territories and some gain over-proportional reproductive success in the iguanas' mating aggregations. Females select males based on size and activity and are thus responsible for the observed mating skew. However, large individuals are strongly selected against during El Ni?o-related famines when dietary algae disappear from the intertidal foraging areas. We showed that differences in algae sward ('pasture') heights and thermal constraints on large size are causally responsible for differences in maximum body size among populations. I hypothesize that body size in many animal species reflects a trade-off between foraging constraints and sexual selection and suggest that future research could focus on physiological and genetic mechanisms determining body size in wild animals. Furthermore, evolutionary stable body size distributions within populations should be analysed to better understand selection pressures on individual body size.     

Phenotypic plasticity of life history traits in relation to reproductive strategies in <Emphasis Type="Italic">Boa constrictor occidentalis</Emphasis>

The close connection between reproductive ecology and life history in snakes leads to trade-offs between reproductive and other life-history traits. Optimal energy allocation to growth and reproduction is a key factor to determine life history structure. Therefore, elucidating the relationship between body size variations and reproductive characters is essential for a better understanding of life-history plasticity. The aim of this work was to determine to what extent life-history differs among populations of Boa constrictor occidentalis and to identify possible life-history trade-offs between morphological and reproductive traits. We compared two populations from areas that are separated latitudinally, with different climatic conditions and vegetation landscape structure. Reproductive and morphological data of specimens were recorded. Although populations had a similar mean length of mature snakes, the frequency of some size classes tended to be different. Size at sexual maturity differed between populations for females, generating variations in the proportion of mature individuals. Reproductive threshold and follicular size also varied, but female reproductive frequency was similar between populations. Reproductive frequency of males varied between populations although their body condition was similar. We discussed two major issues: (1) implications of size at sexual maturity for body size and fecundity; (2) trade-offs in reproductive characters.     

Increasing returns in the life history of Columbian ground squirrels

1. We examined positive associations and trade-offs of maternal and reproductive traits in a population of Columbian ground squirrels, Spermophilus columbianus .
2. Structural size, body condition, mother's personal allocation to body mass during reproduction, and timing of littering were estimated for live-trapped reproductive females that were observed during an 8-year period, and were compared to litter mass, litter size, and average pup mass using path analyses.
3. Mothers exhibited age-structured traits that influenced reproductive patterns. Yearling mothers were significantly smaller, bred later, and had smaller litters than older females. Mothers that gained more body mass during reproduction and older mothers in good body condition that were structurally large had larger litters.
4. Early seasonal timing of littering was an important positive influence on successful reproduction by older mothers only in early breeding seasons and in years when conditions for reproduction were good for all females.
5. The number of offspring that survived to 1 year of age was most strongly associated with litter mass and litter size; date of breeding was of secondary influence, with earlier litters exhibiting greater success.
6. In general, mothers that gained the most in body mass during reproduction were concurrently more successful in weaning large litters (perhaps due to better quality of foraging habitat).
7. In addition to expected reproductive trade-offs, reproduction by Columbian ground squirrels exhibited positive associations of life-history traits that may reflect evolutionary increasing returns.     

Increase in Male Reproductive Success and Female Reproductive Investment in Invasive Populations of the Harlequin Ladybird Harmonia axyridis

Reproductive strategy affects population dynamics and genetic parameters that can, in turn, affect evolutionary processes during the course of biological invasion. Life-history traits associated with reproductive strategy are therefore potentially good candidates for rapid evolutionary shifts during invasions. In a series of mating trials, we examined mixed groups of four males from invasive and native populations of the harlequin ladybird Harmonia axyridis mating freely during 48 hours with one female of either type. We recorded the identity of the first male to copulate and after the 48 h-period, we examined female fecundity and share of paternity, using molecular markers. We found that invasive populations have a different profile of male and female reproductive output. Males from invasive populations are more likely to mate first and gain a higher proportion of offspring with both invasive and native females. Females from invasive populations reproduce sooner, lay more eggs, and have offspring sired by a larger number of fathers than females from native populations. We found no evidence of direct inbreeding avoidance behaviour in both invasive and native females. This study highlights the importance of investigating evolutionary changes in reproductive strategy and associated traits during biological invasions.     

Viability selection on body size in a non-marine ostracod

One of the most important research topics in evolutionary ecology is body size evolution. Actually, several hypotheses have been proposed to explain the many observed patterns—also known as “rules”—of body size variation in across latitude, temperature, and time. The temperature–size rule (TSR), describes an inverse relationship between body size and temperature. We took advantage of the “natural laboratory” that the crustacean populations at the Chilean altiplano offers, to study the TSR in ostracods. We studied three populations of Limnocythere atacamae that are physically separated by several kilometers, and differ mainly by their permanent thermal regime. We found larger individuals in the hotspring compared to the cold ponds. Also, in the hotspring we found a significant quadratic selection coefficient, suggesting stabilizing selection in this population. The fitness profiles showed stabilizing selection in the hotspring, and positive directional selection in the ponds. Our results suggest the existence of an optimal body size above the population means. This optimal size is apparently attained in the hotspring population. Then, natural selection appears to be promoting a shift in the mean phenotype that, for some reason, is not attained in the cold environments. Genetic slippage and population bottleneck would explain this absence of response to selection.     

Comparison of quantitative genetic parameters between two natural populations of a selfing plant species, Medicago truncatula Gaertn.

 In this paper we compare mean values, heritability estimates, coefficient of genetic variation, and genetic correlations among several fitness components of two natural populations of a selfing plant species, Medicago truncatula L. It is shown that the population that had been found most polymorphic for molecular markers in a previous study was also the most variable for quantitative characters. Depending on the traits, the larger heritabilities in this population were due to either larger coefficients of genetic variances or smaller coefficients of environmental variances. Whereas genetic and phenotypic correlation matrices were very similar within each population, they were quite different between populations. In particular, although a positive correlation between age and size at maturity was found in both populations, the correlation between age at maturity and reproductive success was negative in the more variable population (late flowering plant, with a larger size at flowering, produced fewer pods), whereas no correlation was observed in the less variable population. We suggest that while in the less variable population all individuals have a high reproductive effort, several strategies coexist in the more variable population, with some early-flowering genotypes showing a high reproductive effort and other late-flowering genotypes showing a larger competitive ability through increased vegetative growth. Received: 25 June 1996 / Accepted: 11 October 1996     

Variation in selection pressure acting on body size by age and sex in a reverse sexual size dimorphic raptor

Body size strongly influences fitness, with larger individuals benefiting in terms of both greater productivity and survivorship; for reverse sexual size dimorphic (RSD) species, this relationship may be more complex. We examined the selection pressures acting on body size in male and female Merlins Falco columbarius to assess whether larger or smaller individuals of this RSD species were favoured in terms of survival and breeding performance. For males and females there were clear links between body size and survival but the exact relationship varied by sex. Among males, birds that survived each year class were larger than those that died and yearlings were on average smaller than older birds, but there were no measurable differences among adult males (age 2+). Among females, larger individuals aged 1 and 2 years were more likely to survive, but this size‐based pattern was not apparent in older age classes. Size early in life predicted the lifespan in male Merlins but not as strongly as for females and not for the largest individuals. Reproductive performance based on brood size was not associated with body size in either males or females, but there was a weak positive relationship between female body size and lifetime reproductive success. Selection appears to favour larger males and females but there is no indication that the population is evolving towards bigger individuals, perhaps in part due to selection against the largest birds. Increased survival may allow larger and higher quality individuals to occupy higher quality territories as they age and thereby to accrue greater lifetime reproductive success in the process.     

Potential ‘costs of reproduction’ in a skink: Inter‐ and intrapopulational variation

Reproductive costs are important determinants of reproductive effort in squamate reptiles. Consequently, differences in costs of reproduction between populations of geographically or climatically widespread species are likely to result in different patterns of reproductive effort. In the present study, the effect of pregnancy on sprint speed was examined in a small viviparous skink, Niveoscincus ocellatus (Gray 1845), from two populations at the climatic extremes of its distribution. Decreased sprint speed has the potential to be an important cost of reproduction in this species, through a reduced ability to avoid predation and/or decreased foraging efficiency. Lizards inhabiting the colder site were larger than those from the warmer site and, contrary to predictions from life history theory, had a higher reproductive effort. In both populations, sprint speed was lower in pregnant lizards than in either the same individuals after birth or non‐pregnant control lizards. Within each population, sprint speed was unrelated to the level of reproductive effort of the female in terms of either absolute mass of the reproductive burden or the burden relative to her post‐partum body mass. However, within each population, the mass of the clutch that an individual female was carrying relative to snout–vent length was an important determinant of her sprint speed while pregnant. Thus, within each population, a relatively high reproductive burden may potentially increase costs of reproduction in this species. Despite this relationship and predictions from life history theory suggesting that annual reproductive effort will be lower in populations with a large body size and delayed maturity, it is suggested that a higher reproductive effort at the cold site is possible because they have a higher absolute sprint speed because of their larger size and a relatively higher abundance of cover at the cold site, and differences in predation pressure may alter selective pressures on reproductive investment.     

Simulated trapping and trawling exert similar selection on fish morphology

Commercial fishery harvest can influence the evolution of wild fish populations. Our knowledge of selection on morphology is however limited, with most previous studies focusing on body size, age, and maturation. Within species, variation in morphology can influence locomotor ability, possibly making some individuals more vulnerable to capture by fishing gears. Additionally, selection on morphology has the potential to influence other foraging, behavioral, and life‐history related traits. Here we carried out simulated fishing using two types of gears: a trawl (an active gear) and a trap (a passive gear), to assess morphological trait‐based selection in relation to capture vulnerability. Using geometric morphometrics, we assessed differences in shape between high and low vulnerability fish, showing that high vulnerability individuals display shallower body shapes regardless of gear type. For trawling, low vulnerability fish displayed morphological characteristics that may be associated with higher burst‐swimming, including a larger caudal region and narrower head, similar to evolutionary responses seen in fish populations responding to natural predation. Taken together, these results suggest that divergent selection can lead to phenotypic differences in harvested fish populations.     

Old males reduce melanin‐pigmented traits and increase reproductive outcome under worse environmental conditions in common kestrels

Secondary sexual traits displayed by males and females may have evolved as a signal of individual quality. However, both individual quality and investment on producing or maintaining enhanced sexual traits change as individuals age. At the same time, the costs associated to produce sexual traits might be attenuated or increased if environmental conditions are benign or worse respectively. Accordingly, environmental conditions are expected to shape the association between the expression of sexual traits and their reproductive outcome as individuals age. Nonetheless, little is known about the environmental influence on the co‐variation between sexual traits and reproductive outcome throughout the life of individuals. We studied the age‐dependency of the number and size of back spots, a melanin‐based and sexual trait in adults of common kestrels (Falco tinnunculus). We analysed the age‐dependence of reproductive traits and the environmental influence, defined as vole abundance, using a 10‐year individual‐based dataset. We broke down age‐related changes of reproductive traits into within‐ and between‐individual variation to assess their contribution to population‐level patterns. Our results showed a within‐individual decrease in the number, but not the size, of back spots in males. The size of back spots was positively correlated with food availability in males. Reproductive performance of males increased as they aged, in agreement with the life‐history theory but depending of vole abundance. Remarkably, we found that having fewer back spots was positively associated with clutch size only for old individuals under low‐food conditions. We suggest that environmental variation may shape the association between the expression of a sexual signal and reproductive outcome. We speculate that the reliability of sexual traits is higher when environmental conditions are poor only for old individuals. Within an evolutionary context, we suggest that the expression of sexual traits might be constrained by environmental conditions at later stages of life.     

Reproductive strategies and body shape in the European pond turtle (Emys orbicularis) from contrasting habitats in Italy

Comparisons within and among populations offer important insights into variation in life-history traits and possible adaptive patterns to environmental conditions. We present the results of observed differences in body size, body shape and patterns of reproduction in four separate populations of the European pond turtle Emys orbicularis in central and southern Italy – coastal ( n =3) and mountainous ( n =1) sites and pond ( n =2) and canal ( n= 2) habitats – to determine whether phenotypic plasticity affects reproductive output. Although we did not find any significant latitudinal variation in body size, we observed significant differences in body shape between canal (rounded body shape) and pond (elongated body shape) systems and smaller size with rounded shape in the mountainous population. Reproductive output is similar among populations (median=5 eggs per clutch), whereas reproductive investment (relative clutch mass to maternal body mass) is higher in the mountain population (one clutch per year) than in coastal populations (two clutches per year), suggesting differential trade-offs between geographic locality, elevation and habitat type. Turtle shell shape and geographic location together affect reproductive output in E. orbicularis in Italy.     

Probing the adaptive landscape using experimental islands: density-dependent natural selection on lizard body size

Anolis lizards in the Greater Antilles are thought to have diversified through natural selection on body size and shape, presumably due to interspecific competition and variation in locomotor performance. Here we measure natural selection on body size over three years and across seven replicate populations of the brown anole, A. sagrei. We experimentally manipulated an important component of the environment (population density) on several small islands to test the role of density in driving natural selection. Results indicate that the strength of natural selection was proportional to population density (r2 = 0.81), and favored larger body sizes at higher density, presumably owing to the enhanced competitive ability afforded by large size. Changes in the distribution of body size by selective releases of lizards to islands show that this effect did not arise by pure density dependence, since smaller individuals were disproportionately selected against at higher densities. We measured significant broad sense heritability for body size in the laboratory (h2 = 0.55) indicating that selection in the wild could have an evolutionary response. Our results suggest an important effect of population density on natural selection in Anolis lizards.     

Consistent size‐independent harvest selection on fish body shape in two recreationally exploited marine species

Harvesting wild animals may exert size‐independent selection pressures on a range of morphological, life history, and behavioral traits. Most work so far has focused on selection pressures on life history traits and body size as morphological trait. We studied here how recreational fishing selects for morphological traits related to body shape, which may correlate with underlying swimming behavior. Using landmark‐based geometric morphometrics, we found consistent recreational fishing‐induced selection pressures on body shape in two recreationally exploited marine fish species. We show that individuals with larger‐sized mouths and more streamlined and elongated bodies were more vulnerable to passively operated hook‐and‐line fishing independent of the individual's body size or condition. While the greater vulnerability of individuals with larger mouth gapes can be explained by the direct physical interaction with hooks, selection against streamlined and elongated individuals could either involve a specific foraging mode or relate to underlying elevated swimming behavior. Harvesting using passive gear is common around the globe, and thus, size‐independent selection on body shape is expected to be widespread potentially leaving behind individuals with smaller oral gapes and more compact bodies. This might have repercussions for food webs by altering foraging and predation.     

QUANTIFYING EVOLUTIONARY POTENTIAL OF MARINE FISH LARVAE: HERITABILITY,SELECTION, AND EVOLUTIONARY CONSTRAINTS

For many marine fish, intense larval mortality may provide considerable opportunity for selection, yet much less is known about the evolutionary potential of larval traits. We combined field demographic studies and manipulative experiments to estimate quantitative genetic parameters for both larval size and swimming performance for a natural population of a common coral‐reef fish, the bicolor damselfish (Stegastes partitus). We also examined selection on larval size by synthesizing information from published estimates of selective mortality. We introduce a method that uses the Lande–Arnold framework for examining selection on quantitative traits to empirically reconstruct adaptive landscapes. This method allows the relationship between phenotypic value and fitness components to be described across a broad range of trait values. Our results suggested that despite strong viability selection for large larvae and moderate heritability (h²= 0.29), evolutionary responses of larvae would likely be balanced by reproductive selection favoring mothers that produce more, smaller offspring. Although long‐term evolutionary responses of larval traits may be constrained by size‐number trade‐offs, our results suggest that phenotypic variation in larval size may be an ecologically important source of variability in population dynamics through effects on larval survival and recruitment to benthic populations.     

Correlated responses to selection on female egg size in male reproductive traits in a butterfly

Genetic correlations between male and female traits can act as evolutionary constraints and, if involving reproductive traits, potentially influence sexual selection. Artificial selection on egg size in the tropical butterfly Bicyclus anynana has yielded highly divergent lines. Here we report evidence for correlated evolution in male traits. Males from the large-egg selected lines produced significantly heavier spermatophores independent of body size and tended to have more fertile sperm stored in their reproductive tracts than those from the small-egg selected lines. This may be due to an underlying genetic correlation in reproductive effort between the sexes. However, non-fertile sperm number and testis size remained unaffected by selection on egg size. Phenotypic correlations within an unselected population revealed that spermatophore mass and fertile sperm number, but not testis size and non-fertile sperm number, were positively related to male body size, and that larger spermatophores contained more fertile, but not non-fertile sperm. In addition, males provided larger females with bigger spermatophores and more fertile sperm, indicating males may be exercising mate choice during copulation.     

Larger female fish contribute disproportionately more to self-replenishment

While chance events, oceanography and selective pressures inject stochasticity into the replenishment of marine populations with dispersing life stages, some determinism may arise as a result of characteristics of breeding individuals. It is well known that larger females have higher fecundity, and recent laboratory studies have shown that maternal traits such as age and size can be positively associated with offspring growth, size and survival. Whether such fecundity and maternal effects translate into higher recruitment in marine populations remains largely unanswered. We studied a population of Amphiprion chrysopterus (orange-fin anemonefish) in Moorea, French Polynesia, to test whether maternal size influenced the degree of self-recruitment on the island through body size-fecundity and/or additional size-related maternal effects of offspring. We non-lethally sampled 378 adult and young juveniles at Moorea, and, through parentage analysis, identified the mothers of 27 self-recruits (SRs) out of 101 recruits sampled. We also identified the sites occupied by each mother of an SR and, taking into account variation in maternal size among sites, we found that females that produced SRs were significantly larger than those that did not (approx. 7% greater total length, approx. 20% greater biomass). Our analyses further reveal that the contribution of larger females to self-recruitment was significantly greater than expected on the basis of the relationship between body size and fecundity, indicating that there were important maternal effects of female size on traits of their offspring. These results show, for the first time in a natural population, that larger female fish contribute more to local replenishment (self-recruitment) and, more importantly, that size-specific fecundity alone could not explain the disparity.     

BODY SIZE,NATURAL SELECTION,AND SPECIATION IN STICKLEBACKS

There is little evidence from nature that divergent natural selection is crucial to speciation. However, divergent selection is implicated if traits conferring adaptation to alternative environments also form the basis of reproductive isolation. We tested the importance of body size differences to premating isolation between two sympatric sticklebacks. The species differ greatly in size, and several lines of evidence indicate that this difference is an adaptation to alternative foraging habitats. Strong assortative mating was evident in laboratory trials, but a few hybridization events occurred. Probability of interspecific mating was strongly correlated with body size: interspecific spawning occurred only between the largest individuals of the smaller species and the smallest individuals of the larger species. Probability of spawning between similar-sized individuals from different species was comparable to spawning rates within species. Disruption of mating between individuals from different species can be traced to increased levels of male aggression and decreased levels of male courtship as size differences increased between paired individuals. Interspecific mate preferences in sympatric sticklebacks appears to be dominated by body size, implicating natural selection in the origin of species.     

Precocious reproduction increases at the leading edge of a mangrove range expansion

Climate change‐driven shifts in species ranges are ongoing and expected to increase. However, life‐history traits may interact with climate to influence species ranges, potentially accelerating or slowing range shifts in response to climate change. Tropical mangroves have expanded their ranges poleward in the last three decades. Here, we report on a shift at the range edge in life‐history traits related to reproduction and dispersal. With a common garden experiment and field observations, we show that Rhizophora mangle individuals from northern populations reproduce at a younger age than those from southern populations. In a common garden at the northern range limit, 38% of individuals from the northernmost population were reproductive by age 2, but less than 10% of individuals from the southernmost population were reproductive by the same age, with intermediate amounts of reproduction from intermediate latitudes. Field observations show a similar pattern of younger reproductive individuals toward the northern range limit. We also demonstrate a shift toward larger propagule size in populations at the leading range edge, which may aid seedling growth. The substantial increase in precocious reproduction at the leading edge of the R. mangle range could accelerate population growth and hasten the expansion of mangroves into salt marshes.     

Microgeographical variation in brown trout reproductive traits: possible effects of biotic interactions

This study documents substantial variation in reproductive traits among populations of stream-dwelling brown trout ( Salmo trutta L.) at a very small geographic scale. Within two streams, we found a parallel pattern of variation, where females living above major waterfalls produced fewer and larger eggs than conspecifics from below the waterfalls. Four additional streams were represented with either a below-waterfall site ( n =2) or an above-waterfall site ( n =2). When these streams were included in the analyses, there was no consistent difference in reproductive traits between females from above- and below-waterfall sites. There was no significant difference in total reproductive investment among sites within streams, but considerable variation among streams. Female first-year growth rates was estimated from scales, and differed significantly among populations. Within streams, females from below waterfalls experienced higher first-year growth rates as compared to females from above the waterfalls. Within seven out of eight populations, egg size increased significantly with increasing female body length. Within three populations, we found evidence for a trade-off between offspring size and offspring number, as a negative association between fecundity and egg size independently of adult body size. Within three populations egg size decreased significantly with increasing maternal first-year growth, independently of adult body size. We suggest that the within-stream differences in offspring size/number strategies are influenced by population density and growth effects. Earlier, we have shown that population densities are consistently lower below the waterfalls in these streams. The Alpine bullhead ( Cottus poecilopus ) is found only below the waterfalls and could influence brown trout demography.     

Picking personalities apart: estimating the influence of predation,sex and body size on boldness in the guppy Poecilia reticulata

Predation is a strong selective force in most natural systems, potentially fueling evolutionary changes in prey morphology, life history and behaviour. Recent work has suggested that contrasting predation pressures may lead to population differentiation in personality traits. However, there are indications that these personality traits also differ between sexes and not necessarily in a consistent way between populations. We used an integrative approach to quantify boldness (latency to emerge from a shelter) in wild‐caught guppies in relation to predation pressure, population origin, sex and size. In addition we quantified the repeatability of these personality traits. We show that predation regime had significant effects on emergence time. In general, fish from high predation localities emerged sooner from the shelter compared to those from low predation localities. We found strong sex differences; males were significantly bolder than females. The relationship between emergence time and body size was non‐significant in all populations. We discuss what responses to expect from predator‐naïve versus predator‐experienced individuals and how this can be linked to the shyness–boldness continuum.