Fuels for development: evolution of maternal provisioning in asterinid sea stars

For marine invertebrates, larval developmental mode is inseparably linked to the nutritional content of the egg. Within the asterinid family of sea stars there have been multiple, independent, evolutionary transitions to lecithotrophic development from the ancestral, planktotrophic state. To investigate the evolution of maternal investment and development within the Asterinidae, we quantified individual lipid classes and total protein for eggs and larval stages of closely related species representing three developmental modes (planktotrophy, planktonic lecithotrophy and benthic lecithotrophy). Within species, maternal provisioning differed between females indicating that egg quality varied with parentage. Maternal investment was related to egg size but, after correcting for egg volume, we identified two major oogenic modifications associated with the evolution of lecithotrophic development: (1) a reduction in protein deposition that probably reflects the reduced structural requirements of nonfeeding larvae, (2) an increase in deposition of a single class of energetic lipid, triglyceride (TG). The exception was Parvulastra exigua, which has benthic, lecithotrophic development and lays eggs with a lipid to protein ratio close to that of planktotrophs. This oogenic strategy may provide P. exigua larvae with a protein “weight-belt” that assists in maintaining a benthic existence. Asterinids with planktotrophic development used a significant portion of egg TG to build a feeding bipinnaria larva. For Meridiastra mortenseni, female-specific differences in egg TG were still evident at the bipinnaria stage indicating that egg quality has flow-on effects for larval fitness. In lecithotrophic asterinids, TG reserves were not depleted in development to the larval stage whereas protein stores may help fuel early larval development. Available data indicate that there may be two evolutionarily stable egg lipid profiles for free-spawning, temperate echinoderms.     

Predator evasion in a fish school: test of a model for the fountain effect

A model to explain the behavioural mechanisms underlying the fountain manoeuvre, a predator-evasion response shown by fish shoals is tested. It is proposed that the responses of individual fish are constrained by requirements to (1) visually monitor the predator's behaviour, (2) minimise the energetic cost of escape, and (3) maximise the rate of passage around the predator. The model predicts that individuals will swim away from the threat at a constant angle determined by the rear limit of the visual field and that the range of reaction will be constrained by water visibility. The model's predictions were upheld in tests conducted in 1984 using a shoal of juvenile whiting, Merlangius merlangus (L.). It is concluded that the principal determinant of the fountain manoeuvre is the visual field of the fish.     

Mouse lemurs in space and time: a test of the socioecological model

Socioecological theory predicts that the distribution of fertile females in space and time is the major determinant of male spacing behavior and mating strategies. Using a small nocturnal Malagasy primate, the gray mouse lemur (Microcebus murinus), we determined the spatiotemporal distribution of estrous females during the brief annual mating season to examine the predictive power of the socioecological model for male mating strategies. Mouse lemurs are particularly interesting in this respect because this polygynous species is characterized by seasonal reproduction, seasonally reversed sexual dimorphism, and relatively large testes. All resident animals in our 8-ha study area, a total of 30 adult males and 27 adult females, were individually marked and regularly recaptured to determine female reproductive status and to obtain home range data. We found that the mating season is limited to 4 weeks following female emergence from hibernation. Only 3-9 females could have synchronized estruses during a given week, indicating a moderately high male monopolization potential. However, receptive females were not spatially clumped and male ranges overlapped with those of many other rivals. Therefore, we suggest that individual powerful males may be unable to defend exclusive permanent access to receptive females because of prohibitive costs of range defense resulting from the strongly male-biased operational sex ratio and the corresponding intruder pressure. Our general conclusions are (1) that the socioecological model provides a useful heuristic framework for the study of mating systems, but that (2) it does not specify the degree of spatiotemporal clumping of receptive females at which male mating strategies switch among mate guarding, spatial exclusion of rivals, and roaming, and that (3) the operational sex ratio can have profound effects on male mating strategies as well.     

Indiscriminate care of offspring predates the evolution of sociality in alloparenting social spiders

Alloparental care—the care of other’s offspring—is a key aspect of sociality in many groups of animals. Understanding how this complex behavior arises requires identifying both the selective forces that may favor it, as well as characteristics of particular lineages that facilitate or hinder its evolution. One potential hindrance is the existence of discrimination against foreign offspring, an obstacle that would need to be overcome in order for alloparental care to evolve. In this study, we explored whether offspring discrimination may have constrained the evolution of alloparental care in social spiders in the genus Anelosimus. Social spiders are known for their cooperative behaviors, which include alloparental care. After quantitatively assessing the extent of alloparenting in the care of egg sacs in natural nests of these spiders, we investigated whether discrimination against foreign egg sacs existed in ancestral pre-social species in the genus. We did so by testing for discrimination between a female’s own and foreign egg sacs in three subsocial sister taxa of each social species investigated. We found no detectable evidence of discrimination in the care of egg sacs by female Anelosimus, regardless of level of sociality. We used these data, along with those from previous studies, to infer that a lack of discrimination is likely the ancestral state in the genus Anelosimus. This supports the idea that offspring discrimination was not a constraint on the evolution of alloparental care in social Anelosimus species. We discuss the evolutionary implications of this finding, and suggest that lack of offspring discrimination may have eased the transition from solitary to cooperative breeding.     

The evolution of female copulation calls in primates: a review and a new model

Female copulation calls are mating-associated vocalizations that occur in some species of Old World monkeys and apes. We argue that copulation calls have two immediate functions: to encourage mating attempts by other males and to increase mate guarding by the consort male. We hypothesize that female copulation calls have evolved under the selective pressures of risk of infanticide and sperm competition. When male mate guarding is effective, copulation calls allow females to concentrate paternity in dominant males and benefit from their protection against the risk of infanticide. When mate guarding is ineffective, copulation calls may bring genetic benefits to females through facilitation of sperm competition. We present a quantitative model in which interspecific variation in females' promiscuity predicts their tendency to use copulation calls in conjunction with mating. The model predicts that in species with little female promiscuity, copulation calls should be rare and exhibited only in association with mating with dominant males. In species in which females are highly promiscuous, copulation calls should be frequent and unrelated to male dominance rank. The limited data available to test the model support its main predictions as well as the predicted relation between copulation calls and male dominance rank.

Sexual selection and the evolution of bird song: A test of the Hamilton-Zuk hypothesis

Summary Hamilton and Zuk (1982) suggested that secondary sexual characters evolve because they allow females to assess a potential mate's ability to resist parasites. A prediction of this theory is that the degree of elaboration of secondary sexual characters should be positively correlated with parasite load across species. In support of their hypothesis, Hamilton and Zuk reported a correlation across North American passerine species between haematozoa prevalence and both brightness and song complexity and variety, scored on a subjective six point scale. Here we show that this relationship is confounded by phylogenetic associations. We use quantitative data on song duration, inter-song interval, song continuity, song rate, song versatility, and song and syllable repertoire size for 131 species of European and North American passerines to test the Hamilton-Zuk hypothesis. Across species, there are significant negative relationships between haematozoa prevalence and song continuity, contrary to the direction predicted by Hamilton and Zuk. In accordance with their prediction, there is a positive correlation with song versatility. However, these relationships come about through taxonomic associations: within taxa there are no consistent relationships between any of the song variables and haematozoa prevalence. None of the other song variables correlate with haematozoa prevalence. We conclude that there is no evidence of an association between song elaboration and parasites. Offprint requests to: A.F. Read     

Mate choice tactics and swarm size: a model and a test in a dance fly

In the dance flyEmpis borealis (L.) (Diptera: Empididae) females gather to swarm and males visit swarms for mating. A model was constructed, based on previously published data, simulating how males may choose among females of different sizes in swarms of different sizes. The focal question was, what influences the number of individuals in the swarm in this and possibly other swarming insects? The relationships between original swarm size and both the number of males arriving per minute and the proportion of males mating are both logarithmic. The model predicted that if these relationships were linear, or if males were able to judge absolute female size, the mean swarm size should increase and be at least four times as large as those found in the field. The only type of male mate choice strategy that gave rise to very large swarms (>25) was size-related choice (if males are able to assess the size of a female in relation to the entire population and not merely to the swarm). Furthermore, no swarming behaviour would occur if males mate independently of swarm size. Thus, the numbers of females attending a given swarm site are influenced by male arrival pattern, male preference for larger swarms, the inability of males to judge the absolute body size of females, and female polyandry. Males searching for mates seem to prefer larger swarms than females searching for a swarm to join, but the mean swarm size is primarily set by the swarm size preference of females. Optimal swarm size predicted from the model was 4.68±0.53 females. In order to test model predictions, 69 natural swarm sites were studied during one season. The mean swarm size was 4.85±4.54 females (median 4.03), and about 90% of swarms consisted of 11 females or fewer. Predicted and observed swarm size did not differ significantly.     

Development and test of a crop growth model for application within a Global Change decision support system

When examining potential impacts of Global Change on water resources on the regional scale, spatial and temporal changes in crop water and nitrogen demand are of fundamental significance. State-of-the-art crop growth models are powerful tools to assess the response of crops to altered environmental conditions and cultivation practices. In this paper, the process-based, object-oriented and generic DANUBIA crop growth model is presented. To evaluate the performance of the model, a validation analysis is carried out by comparing modelled data with various field measurements of sugar beet, spring barley, maize, winter wheat and potato crops. Model performance statistics show that crop growth is efficiently simulated. The closest agreement between measured and modelled biomass and leaf area index is achieved for sugar beet and winter wheat. Additionally, the response of the model to changed nitrogen availability caused by cultivation practices is analysed and reveals good results. The results suggest that the model is a suitable tool for numerically assessing the consequences of Global Change on biomass production, water and nitrogen demand, taking into account the complex interplay of water, carbon and nitrogen fluxes in agro-ecosystems.     

The number of males in primate social groups: a comparative test of the socioecological model

As applied to polygynous mammals, the socioecological model assumes that environmental risks and resources determine the spatial and temporal distribution of females, which then sets male strategies for monopolizing fertile matings. The effects of female spatial distribution (i.e., female number) and temporal overlap (female mating synchrony) have been examined in comparative studies of primates, but the relative influence of these two factors on male monopolization potential (the number of males) remains unclear. One particular problem is that female synchrony is more difficult to estimate than female number. This paper uses multivariate statistical methods and three independent estimates of female synchrony to assess the roles of spatial and temporal effects in the context of a phylogenetically corrected dataset. These analyses are based on sensitivity analyses involving a total of four phylogenies, with two sets of branch length estimates for each tree, and one nonphylogenetic analysis in which species values are used (because male behavior may represent a facultative response to the distribution of females). The results show: (1) that breeding seasonality predicts male number (statistically significant in six out of nine sensitivity tests); (2) that expected female overlap, after controlling for female group size using residuals, also accounts for the number of males in primate groups (significant in eight out of nine tests), and (3) that actual estimates of female mating synchrony predict male number, again after correcting for female group size (significant in five out of nine tests). Nonsignificant results are in the predicted direction, and female group size is significant in all statistical tests. These analyses therefore demonstrate an independent influence of female temporal overlap on male monopolization strategies in mammalian social systems. Received: 24 July 1998 / Received in revised form: 5 February 1999 / Accepted: 7 February 1999     

Maternal provisioning for larvae and larval provisioning for juveniles in the toxopneustid sea urchin <Emphasis Type="Italic">Tripneustes gratilla</Emphasis>

Lipid and protein biochemistry of eggs (84 μm in diameter), embryos and early larvae of the tropical echinoid Tripneustes gratilla (Linnaeus 1758) were quantified to determine how maternal provisions are used to fuel development of the echinopluteus. The eggs contained a mean of 30.82 ng lipid and 87.32 ng protein. Energetic lipids were the major lipid component (55.52% of total lipid) with the major class being triglyceride (TG: mean 15.9 ng, 51.58% of total). Structural lipid was dominated by phospholipid (PL: mean 11.18 ng, 36.26% of total). Early embryogenesis was not a major drain on egg energetic lipid and protein. Development of the functional feeding larva used ca. 50% of initial egg energetic lipid and most of this was TG. Maternal TG was still present in the 8-day echinoplutei and it was estimated that this energetic lipid would be depleted in unfed larvae by day 10. There was no change in PL. In a separate experiment lipid biochemistry of rudiment stage larvae and early developing juveniles were quantified to determine how lipids are used during metamorphosis. Fed larvae accumulated lipid (mean 275.49 ng) with TG and PL being the major energetic and structural lipids, respectively. Larval lipid stores were not appreciably depleted by metamorphosis and so were available for the early benthic stage juvenile. Juveniles started their benthic existence with 314 ng total lipid (TG: mean 46.84 ng, 14.9% of total, PL: mean 137.51 ng, 43.67% of total). Nile Red histochemistry and histology showed that the stomach serves as a nutrient storage organ and, that lipid stores accrued by larvae sustain developing juveniles for up to 4 days post settlement. Triglyceride supported both non-feeding stages of development and the prefeeding larval and perimetamorphic benthic stage. In this first study of lipid stores in settlement stage echinoderm larvae, we show that T. gratilla larvae sequester the same major energetic lipid (TG) to support the early juvenile that the female parent provided them to fuel early development.     

A model for the evolution of communal foraging in hierarchically structured populations

A kin selection model is described for populations in which groups of interacting individuals (trait groups, sensu Wilson 1975) are spatially situated within larger aggregations. The model predicts the optimal foraging strategy when resources are shared with other trait group members and there is an individual risk in foraging. The ecological mechanism of variation in group fitness, differential resource accumulation, is explicitly incorporated into the model. The optimal foraging rate obtained from this model depends on the product of a benefit-to-cost ratio and a relatedness parameter. The appropriate definition of relatedness for the evolution of communal foraging is determined by the details of the ecological interaction between consumers and resources. When competition is purely intra-specific, the genetic correlation among interactants relative to other members of the local aggregation defines the relatedness parameter applicable to selection on foraging propensity. When competition is primarily inter-specific, the genetic correlation among trait group members relative to the entire population defines relatedness.     

Paternal care in the European starling,Sturnus vulgaris: nestling provisioning

The extent to which male birds in polygynous species with biparental care assist in nestling feeding often varies considerably between nests of different mating status. Both how much polygynous males assist and how they divide their effort between nests may have a profound effect on the evolution of mating systems. In this study we investigated how males in the facultatively polygynous European starling Sturnus vulgaris invested in their different nests. The amount of male assistance affected the quality of the offspring. Polygynous males invested as much as monogamous males, but divided their effort asymmetrically between nests, predominantly feeding nestlings of first-mated (primary) females. Although females partly compensated for loss of male assistance, total feeding frequency was lower at primary females’ nests than at monogamous females nests. Secondary females received even less assistance with nestling rearing, and the extent to which males assisted decreased with the length of the interval between the hatching of the primary and secondary clutches. These results are contrasted with those from a Belgian populations of starlings with a much more protracted breeding season and thus greater opportunities for males to attract additional mates during the nestling rearing period. The results show that both the “defence of male parental investment model” and the “asynchronous settlement model” have explanatory power, but that their validity depends on the potential length of the breeding season. Received: 21 July 1995/Accepted after revision: 13 July 1996     

Experimental test of the pupation window model for development of detritivorous insects

Cohort size and food availability to larval detritivores are linked to pupal mass, and hence to adult fitness, by the pupation window model. Previous tests of this model have employed artificial food. This paper derives a version of the model that incorporates the dynamics of natural detritus. Tests of the model using cohorts of Aedes triseriatus Say led to successful predictions of numbers of pupae, female pupal mass, and female development time. However, it is recommended that model parameters be estimated separately for different types of leaf litter.     

The model of long-term evolution of the carbon cycle

The weathering processes and their role in the formation of the atmospheric carbon and, as a consequence, on the climate are considered. The model operates in the framework of “active planetary cover”, i.e. considering the interactive role of the biosphere, looking at its development as a non-linear evolutionary system of so-called “virtual biospheres”.     

Experimental evidence for food limitation and sex-specific strategies of American kestrels (<Emphasis Type="Italic">Falco sparverius</Emphasis>) provisioning offspring

For birds with altricial young, the brood-rearing period is one of the most energetically expensive periods in their lives and may be the bottleneck for fitness. Because parents are expected to be prudent in allocating resources between reproduction and self-maintenance, food supply should be an important factor determining reproductive decisions during brood rearing. Parents with abundant food are expected to have enhanced fitness because they are able to reduce their work rates and increase their own survival chances, because their offspring may be of higher quality, or some combination of these. However, few studies have simultaneously documented all of these variables in a single investigation. We performed a food supplementation experiment to test how food supply influenced provisioning decisions by parent American kestrels (Falco sparverius). Female kestrels showed a strong response to extra food and reduced their provisioning rates. As a result, supplemented females had higher return rates than control females, suggesting significant effects of food on female survival. Because females used extra food to increase their fitness, our results suggest that kestrels raising offspring are limited by food. Male kestrels whose nests were supplemented also responded to extra food by reducing provisioning, but to a much lesser extent than their mates. Male parents did not appear to benefit from supplementation, as their return rates were similar to control males. The total amount of food received on a daily basis by nestlings was similar between supplemented and control nests. Supplemented offspring therefore did not fledge in better condition or have higher survival rates than control nestlings; the only significant factor consistently affecting offspring condition and survival was weather.     

Sex-specific maternal investment in pronghorn,and the question of a limit on differential provisioning in ungulates

Summary Prediction that mothers will invest more in individual sons than daughters in polygynous mammals has been confirmed in several species. However, among polygynous ungulates, differential investment occurs in some species, but not in others. Because ungulates have postnatal growth rates among the highest in mammals, we hypothesized that level of maternal investment limits the ability of offspring of one sex to evolve faster growth rates, even when intrasexual selection might favor faster growth. We predicted that comparative rate of maternal investment would explain the distribution of differential investment among ungulates, and examined our data on pronghorn (Antilocapra americana), which show the highest-known rate of maternal investment among ungulates. Data on birth weights, suckling rates, ages-pecific frequency of maternal termination of suckling bouts, age at weaning, and rate of rejected suckle attempts showed either no sex differences or else a slight excess investment in daughters. In concordance with these data, female fawns spent more energy in activity than did male fawns. Among ungulates for which data are available, the best predictor of differential investment is not degree of adult sexual dimorphism; it is comparative rate of maternal investment.     

Ectoparasites of house sparrows (Passer domesticus): an experimental test of the immunocompetence handicap hypothesis and a new model

Conspicuous secondary sexual traits may have evolved as handicap-revealing signals or as badges of status. We present results of an experiment using males of the sexually dimorphic house sparrow (Passer domesticus), that support the idea that the male-specific bib can be both a handicap-revealing signal and a reliable badge indicating the physical condition of the bird. In a test of the immunocompetence handicap hypothesis, wild-caught adult male house sparrows were studied in captivity. Birds implanted with elevated doses of testosterone were more dominant, had higher circulating levels of both testosterone and corticosterone and they also harboured relatively larger ectoparasite loads. Higher parasite loads were also associated with individuals showing lower immunocompetence and larger changes in bib size. A new model for immunocompetence effects in sexual selection is introduced, integrating actions that the hypothalamopituitary axis exerts on gonads, adrenals and the thyroid gland. The ”integrated immunocompetence model” synthesizes both the ”handicap” (i.e. survival-decreasing) and ”badge of status” (i.e. survival- enhancing) models for evolution of secondary sexual traits. Received: 15 May 1999 / Received in revised form: 2 November 1999 / Accepted: 6 November 1999     

Inter-male competition for high-quality host-plants: the evolution of protandry in a territorial grasshopper

Summary Males of the desert grasshopper Ligurotettix coquilletti typically eclose 3–5 weeks prior to females. Early-eclosed males experience more female encounters than the later-eclosed individuals. Evidence suggests that the number of encounters may be proportional to male lifetime mating success. Early-eclosed males enjoyed greater adult lifespans, occupied and defended higher quality territories (Larrea shrubs), and tended to be dominant on these shrubs if several males were present. The elevated number of female encounters were not conferred on early-eclosed males by their extended survivorship, but rather by the high quality of their territories, which retained numerous females, and their dominant behavior. We evaluate several female-benefit and male-benefit hypotheses for the evolution of protandry and propose that in L. coquilletti, the phenomenon arose due to male-male competition for female-encounter sites, a mechanism not considered in earlier models. Finally, we discuss several reasons for the high variance in the date of male eclosion.