Alternative Reproductive Strategies Research Articles

Differential investment and size-related mating strategies facilitate extreme size variation in contesting male spiders

Sexually selected variation in male body size is often associated with alternative reproductive strategies that may persist under frequency-dependent selection or result from ‘making the best of a bad job’ in inferior individuals. The spider genus Nephila is well known for female gigantism and male dwarfism, serving as an established model system to investigate selection on male size and the still enigmatic sexual size dimorphism (SSD). Less attention has been paid to the enormous size variation among males that exists in some Nephila species despite broad evidence for large male advantages in contest competition. As the existing variation contradicts strongly biased fitness returns among different phenotypes, detailed investigations of fitness consequences related to different body sizes and their associated mating strategies are required. We used the African golden-silk spider Nephila senegalensis to test whether size-dependent alternative mating strategies yield equivalent reproductive success in dyads of size-mismatched males competing for a single female. Our results confirm that differently sized males achieve similar paternity and reveal complex interrelations between competing strategies, which mutually influence each other. Males integrate their own competitive ability, the intensity of sperm competition and female reproductive value to adjust their mating investment accordingly. Size-related mating strategies, combined with behavioural flexibility, may thus promote the maintenance of male size variation by balancing fitness returns and exemplify how changes in selective context can dissolve the principal large-size benefits. We suggest that flexible adaptive responses may significantly contribute to stabilizing SSD.

Unintentional selection, unanticipated insights: introductions, stocking and the evolutionary ecology of fishes.

Natural environmental change has produced countless opportunities for species to disperse into and persist in habitats where they previously did not exist. Introduction and stocking programmes have facilitated similar sorts of colonization opportunities across considerably greater geographical scales and often in much shorter periods of time. Even though the mechanism of colonization differs, the result can be the same: evolutionary change in the colonizing population in response to novel selection pressures. As a consequence, some human-mediated fish transfers have unintentionally yielded novel research opportunities to study how phenotypes and genes interact with their environment and affect ecological and evolutionary change. The primary purpose here is to explore how work, directly or indirectly involved with human-mediated transfers, has unintentionally yielded novel research and research opportunities in fish ecology and evolution. Insights have produced new knowledge or altered previously held perceptions on topics such as local adaptation, rate of evolutionary change, phenotypic plasticity, alternative reproductive strategies, population structure and colonization probability. Well-documented stocking programmes, especially in terms of history, numbers and original population sources, can provide highly fertile ground for generating further insights on the ecology and evolution of fishes and of the factors likely to influence the success of conservation-based, restoration programmes.

An evolutionary perspective on conflict and compensation in physiological and functional traits

Abstract Physiological and functional traits, especially those related to behavior and whole-organism performance capacities, are subject to a variety of both parallel and opposing natural and sexual selection pressures. These selection pressures show considerable interspecific variation, shaping contemporary behavioral and functional diversity, but the form and intensity of selection on physiological and functional traits can also vary intraspecifically. The same suites of traits can experience quite different selection pressures, depending on the sex or age of a given individual, as well as the presence and nature of alternative reproductive strategies and tactics. These interand intra-locus genetic conflicts have potentially important consequences for the evolutionary trajectories of traits subject to them. Consequently, any intraspecific conflicts which could displace traits from their selective optima in certain classes of individuals relative to others are expected to result in selection for mechanisms to compensate for deviation from those optima. Such conflicts include interlocus sexual conflict, intralocus sexual conflict, and interacting phenotypes, as well as conflict within a sex. In this paper, we consider the evidence for, and implications of, such conflicts for physiological and functional traits in diverse taxa, including both vertebrates and invertebrates, and evaluate the various mechanisms, ranging from behavioral and mechanical to energetic and genetic, enabling compensation. We also discuss how preand post-mating conflicts, as well as interacting phenotypes, might affect the evolution of behavior and physiological and functional traits. Investigators that seek to understand the links among behavior, morphology, physiology, and function should consider such conflicts.

Ontogeny of the proliferous spikelet inEleocharis viridans(Cyperaceae)

Cyperaceae, the third largest family of monocotyledons, show unusual asexual reproductive strategies, such as pseudovivipary involving the formation of new individuals from somatic tissues of floral structures. In Eleocharis pseudovivipary is an important reproductive process in series Tenuissimae, which results in a structure called a proliferous spikelet. With the aim of describing the ontogenetic process of the pseudovivipary in E. viridans, proliferous spikelets at different developmental stages were analysed by light microscopy and scanning electron microscopy. The proliferous spikelet develops from a meristem located in the axil of the basal glume, homologous to bracts of other groups of Cyperaceae, in the culm of the parental plant. Each proliferous spikelet is formed by sympodial units, which consist of an addorsed prophyll, an outer and inner sheath and a culm, which develops a primordium of floriferous spikelet at the terminal region, which can be aborted, and may develop a proliferous spikelet lateral in the axil of the basal glume. The second internode of each sympodial unit contains a root primordium and an intercalary meristem at the culm base. Our results indicate that pseudovivipary can coexist with sexual reproduction as an alternative reproductive strategy, allowing the rapid spread of populations.

A likelihood-based approach for assessment of extra-pair paternity and conspecific brood parasitism in natural populations.

Genotypes are frequently used to assess alternative reproductive strategies such as extra-pair paternity and conspecific brood parasitism in wild populations. However, such analyses are vulnerable to genotyping error or molecular artefacts that can bias results. For example, when using multilocus microsatellite data, a mismatch at a single locus, suggesting the offspring was not directly related to its putative parents, can occur quite commonly even when the offspring is truly related. Some recent studies have advocated an ad-hoc rule that offspring must differ at more than one locus in order to conclude that they are not directly related. While this reduces the frequency with which true offspring are identified as not directly related young, it also introduces bias in the opposite direction, wherein not directly related young are categorized as true offspring. More importantly, it ignores the additional information on allele frequencies which would reduce overall bias. In this study, we present a novel technique for assessing extra-pair paternity and conspecific brood parasitism using a likelihood-based approach in a new version of program cervus. We test the suitability of the technique by applying it to a simulated data set and then present an example to demonstrate its influence on the estimation of alternative reproductive strategies.

Fire salamander (Salamandra salamandra) in Larzac plateau: low occurrence, pond-breeding and cohabitation of larvae with paedomorphic palmate newts (Lissotriton helveticus)

th November; revised on 2014, 18 th January; accepted on 2014, 31 st January Abstract. Alternative reproductive strategies are widespread in caudate amphibians. Among them, fire salamanders (Salamandra salamandra) usually rely on streams to give birth to aquatic larvae but also use ponds, whereas palmate newt larvae (Lissotriton helveticus ) typically metamorphose into terrestrial juveniles, but can also reproduce in retain- ing their gills, a process known as paedomorphosis. Here we report repeated observations of an unusual case of coex- istence of these two alternative traits in the same pond (Larzac, France). The prevalence of fire salamanders in South- ern Larzac was very low (pond occupancy: 0.36%). The observed abundance of fire salamander larvae and paedo- morphic newts was also low in the studied pond. On one hand, the rarity of this coexistence pattern may suggest that habitat characteristics may not be optimal or that competition or predation processes might be operating. However, these hypotheses remain to be tested. On the other hand, as this is the only known case of breeding in Southern Lar - zac, it could be considered to be at a high risk of extirpation.

Criminal offending as part of an alternative reproductive strategy: investigating evolutionary hypotheses using Swedish total population data

Criminality is highly costly to victims and their relatives, but often also to offenders. From an evolutionary viewpoint, criminal behavior may persist despite adverse consequences by providing offenders with fitness benefits as part of a successful alternative mating strategy. Specifically, criminal behavior may have evolved as a reproductive strategy based on low parental investment reflected in low commitment in reproductive relationships. We linked data from nationwide total population registers in Sweden to test if criminality is associated with reproductive success. Further, we used several different measures related to monogamy to determine the relation between criminal behavior and alternative mating tactics. Convicted criminal offenders had more children than individuals never convicted of a criminal offense. Criminal offenders also had more reproductive partners, were less often married, more likely to get remarried if ever married, and had more often contracted a sexually transmitted disease than non-offenders. Importantly, the increased reproductive success of criminals was explained by a fertility increase from having children with several different partners. We conclude that criminality appears to be adaptive in a contemporary industrialized country, and that this association can be explained by antisocial behavior being part of an adaptive alternative reproductive strategy.

High Urban Breeding Densities Do Not Disrupt Genetic Monogamy in a Bird Species

Urbanization causes widespread endangerment of biodiversity worldwide. However, some species successfully colonize cities reaching higher densities than in their rural habitats. In these cases, although urban city dwellers may apparently be taking advantage of these new environments, they also face new ecological conditions that may induce behavioural changes. For example, the frequency of alternative reproductive behaviours such as extra-pair paternity and intraspecific brood parasitism might increase with breeding densities. Here, using a panel of 17 microsatellites, we tested whether increments in breeding densities such as those associated with urban invasion processes alter genetic monogamy in the burrowing owl Athene cunicularia. Our results show low rates of extra-pair paternity (1.47%), but relatively high levels of intraspecific brood parasitism (8.82%). However, we were not able to detect differences in the frequency at which either alternative reproductive behaviour occurs along a strong breeding density gradient. Further research is needed to properly ascertain the role of other social and ecological factors in the frequency at which this species presents alternative reproductive strategies. Meanwhile, our results suggest that genetic monogamy is maintained despite the increment in conspecific density associated with a recent urban invasion process.

Breeding Experience, Alternative Reproductive Strategies and Reproductive Success in a Captive Colony of Zebra Finches (Taeniopygia guttata)

Birds exhibit a remarkable diversity of different reproductive strategies both between and within species. Species such as the zebra finch (Taeniopygia guttata) may evolve the flexible use of alternative reproductive strategies, as well as benefit from prior breeding experience, which allows them to adaptively respond to unpredictable environments. In birds, the flexible use of alternative reproductive strategies, such as extra-pair mating, has been reported to be associated with fast reproduction, high mortality and environmental variability. However, little is known about the role of previous breeding experience in the adaptive use of alternative reproductive strategies. Here we performed an in-depth study of reproductive outcomes in a population of domesticated zebra finches, testing the impact of prior breeding experience on the use of alternative reproductive strategies and reproductive success. We provide evidence that older females with prior breeding experience are quicker to initiate a clutch with a new partner and have increased success in chick rearing, even in a captive colony of zebra finches with minimal foraging demands. We also find evidence that the breeding experience of other females in the same social group influences reproductive investment by female zebra finches. Furthermore, we demonstrate that the use of alternative reproductive strategies in female zebra finches is associated with previous failed breeding attempts with the same pair partner. The results provide evidence that age and breeding experience play important roles in the flexible use of both facultative and adaptive reproductive strategies in female zebra finches.

Occurrence of extra-pair paternity and intraspecific brood parasitism in the Whiskered Tern Chlidonias hybrida

Capsule Patterns of parentage were studied in a colony of Whiskered Terns Chlidonias hybrida in central Poland. We assessed the parentage of 64 chicks from 30 broods using five polymorphic microsatellite loci. The rate of extra-pair paternity was estimated at 8.1% of offspring and 11.8% of broods (the upper 95% CL: 16.9% and 27.1%, respectively), whereas intraspecific brood parasitism was recorded in 4.7% of offspring and 10.0% of broods (the upper 95% cl: 9.9% and 20.7%, respectively). The data obtained on the occurrence of alternative reproductive strategies in Whiskered Tern are consistent with general patterns of parentage found in other colonial larids.

Low historical rates of cuckoldry in a Western European human population traced by Y-chromosome and genealogical data.

Recent evidence suggests that seeking out extra-pair paternity (EPP) can be a viable alternative reproductive strategy for both males and females in many pair-bonded species, including humans. Accurate data on EPP rates in humans, however, are scant and mostly restricted to extant populations. Here, we provide the first large-scale, unbiased genetic study of historical EPP rates in a Western European human population based on combining Y-chromosomal data to infer genetic patrilineages with genealogical and surname data, which reflect known historical presumed paternity. Using two independent methods, we estimate that over the last few centuries, EPP rates in Flanders (Belgium) were only around 1–2% per generation. This figure is substantially lower than the 8–30% per generation reported in some behavioural studies on historical EPP rates, but comparable with the rates reported by other genetic studies of contemporary Western European populations. These results suggest that human EPP rates have not changed substantially during the last 400 years in Flanders and imply that legal genealogies rarely differ from the biological ones. This result has significant implications for a diverse set of fields, including human population genetics, historical demography, forensic science and human sociobiology.

Drifting behaviour as an alternative reproductive strategy for social insect workers

Restricted reproduction is traditionally posited as the defining feature of eusocial insect workers. The discovery of worker reproduction in foreign colonies challenges this view and suggests that workers' potential to pursue selfish interests may be higher than previously believed. However, whether such reproductive behaviour truly relies on a reproductive decision is still unknown. Workers' reproductive decisions thus need to be investigated to assess the extent of workers' reproductive options. Here, we show in the bumblebee Bombus terrestris that drifting is a distinct strategy by which fertile workers circumvent competition in their nest and reproduce in foreign colonies. By monitoring workers' movements between colonies, we show that drifting is a remarkably dynamic behaviour, widely expressed by both fertile and infertile workers. We demonstrate that a high fertility is, however, central in determining the propensity of workers to enter foreign colonies as well as their subsequent reproduction in host colonies. Moreover, our study shows that the drifting of fertile workers reflects complex decision-making processes associated with in-nest reproductive competition. This novel finding therefore adds to our modern conception of cooperation by showing the previously overlooked importance of alternative strategies which enable workers to assert their reproductive interests.

Extra-pair copulations, intra-specific brood parasitism, and quasi-parasitism in birds: a theoretical approach

Although 90 % of all bird species are monogamous, many species practice alternative reproductive strategies as extra-pair copulations, intra-specific brood parasitism, and quasi-parasitism. In territorial monogamous species, both partners hold and defend the territory from intruders. Often, the intruders are males and usually the local male banishes the intruders. Indeed, many studies focused on the response of the local male toward intruder males. However, the benefits and costs associated with the responses of the local male toward intruder females have been largely overlooked. Focusing mainly on alternative reproductive strategies, we developed a model to predict the aggression a monogamous male may demonstrate toward an intruder female during the pre-egg laying stage of his local female partner. This model demonstrates that the intensity of aggression that the local male shows toward an intruder female depends on the extra-pair copulations that his local female partner may perform. Further, the aggression also depends upon intra-specific brood parasitism and quasi-parasitism that might be carried out by the intruder female. Our approach suggests that when considering mating strategies, there is a need to assess how these three alternative reproductive strategies may affect the local male's aggression toward intruder females.

The effect of intruders on territorial Palestine Sunbirds (Nectarinia osea) during the pre-egg laying period

In monogamous species, conspecific aggression is a primary tactic to deter intruders. Alternative reproductive strategies, such as extra-pair copulations or intra-specific brood parasitism that peak at the pre-egg laying period and are practised by intruders, pose a significant threat to the monogamous pair. Here, we addressed the question whether male and female Palestine Sunbirds (Nectarinia osea) demonstrate different aggression levels toward conspecific intruders during the pre-egg laying period. We further asked whether indirect measures of certainty of paternity affect male aggression toward such intruders. For that, we measured the aggression of both partners toward intruders while using stuffed birds. We conducted two experiments on a monogamous and territorial Palestine Sunbird population. In the first experiment, we exposed breeding pairs to a conspecific or a heterospecific intruder and measured their aggression toward it. During the second experiment, we exposed breeding pairs to an intruder, before and after temporarily removing the local male. The local male demonstrated higher aggression than the local female toward a male decoy. Toward a female decoy, the local male demonstrated lower aggression than the local female. Following their release, the removed males did not change their aggression toward the male decoy, but rather they decreased their aggression toward the female decoy. These results suggest that the indirect male’s certainty of paternity may be an important factor of the male’s interests when he faces a risk of potential intra-specific brood parasitism. Furthermore, these findings suggest that each gender is more sensitive to its similar intruder gender, and acts according to its interests in terms of its aggression toward the intruder.

An Experimental Study of the Gestation Costs in a Viviparous Lizard: A Hormonal Manipulation

The trade-offs between reproduction and survival or future reproduction represent the costs of reproduction, which are central to the theory of life-history traits evolution. In particular, different stages of the reproductive cycle may be associated with different costs and thus explain the evolution of alternative reproductive strategies. Viviparity (live bearing) has evolved from oviparity (egg laying) several times independently in vertebrates. To better understand these transitions, we aimed to specifically investigate gestation costs in a squamate reptile with a new experimental procedure. We reduced litter size during gestation in the common lizard (Zootoca vivipara) with a hormonal injection of arginine vasotocin. This method is less invasive than a surgical method and does not reduce the number of offspring of future reproductive events. We monitored body mass change, immune response, endurance capacity, thermoregulatory behavior, offspring characteristic at birth, female and offspring survival, female body mass gain after parturition, and offspring growth rate after birth. Maternal treatment did not significantly change the offspring characteristics measured. Thus, litter size reduction did not change offspring development during gestation. For the females, there is evidence that endurance capacity during gestation is modified because of the physical burden of the litter and because of physiological changes. With respect to gestation costs, we did not observe a trade-off between the investment during gestation and females' resources postparturition (female body mass) or survival, but there was a facultative trade-off with the immune response. It will be interesting to replicate this study to increase the robustness of these results and to confirm the effects on the endurance capacity and the immune response. Gestation costs seem to be limited in this species, and they should be studied in more detail to evaluate their influence on the evolution of viviparity.

Nutrition during sexual maturation affects competitive ability but not reproductive productivity in burying beetles

Summary Food availability can be unpredictable. When food becomes more abundant following a period of low food availability, developing larvae or juveniles often allocate resources preferentially towards increasing growth. This has important long‐term effects on adult phenotypes and longevity. Despite the importance of strategic resource allocation during early development, few studies have examined how changes in resource availability during other windows of development affect reproductive strategies and fitness independent of growth. We manipulated food availability in a burying beetle, Nicrophorus vespilloides, during a subadult period of sexual maturation when individuals cannot increase structural size but are still undergoing reproductive maturation. In contrast to the trade‐offs during larval or juvenile growth, beetles that experienced delayed feeding during reproductive maturation allocated resources preferentially towards maintaining both reproductive function and longevity. In both sexes, delayed feeding beetles were much less successful in competition for carcasses. However, delayed feeding males and females provided similar amounts of parental care and did not differ in reproductive success or longevity. These results indicate that the nutritional environment experienced during a key developmental window may be an important determinant of the expression of alternative reproductive strategies in adulthood, independent of body size.

Immune and oxidative stress trade-offs in four classes of Ruffs (Philomachus pugnax) with different reproductive strategies

Immunity and resistance to oxidative stress are two mechanistically related aspects of self-maintenance that are usually not studied together in connection to ecological or evolutionary relevant variables. Whereas many studies compare two sexes, here we use Ruffs (Philomachus pugnax (L., 1758)), a species in which males have three alternative reproductive morphs: independents, satellites, and faeders. Previous work suggested that immune function in Ruffs depends on energetic constraints or potential of injuries. Based on their behaviour and life history, the three male morphs and females can be placed on an ordinal scale with independents at one end and females at the other, and these two explanations predict opposite patterns along this continuum. Innate and cell-mediated immunity decreased along this axis from independents to females, supporting a risk-of-injury explanation over the energetic constrains hypothesis. No such pattern was evident for oxidative stress or resistance, and no relationship was detected between immunity and oxidative resistance or stress. Hence, during the breeding season immunity reflected the risk of injury, with faeders located in the immunological continuum between females and other male morphs. Species with alternative reproductive strategies provide particularly useful systems in which to address the evolution and ecology behind physiological mechanisms.

Conspecific Brood Parasitism in the White‐faced Ibis Plegadis chihi (Aves: Pelecaniformes) Revealed by Microsatellites' Based Kinship‐Reconstruction

The white-faced ibis Plegadis chihi Vieillot, 1817 (Pelecaniformes: Threskiornithidae) is a socially monogamous colonially breeding bird in which behavioral and ecological observations suggest the occurrence of conspecific brood parasitism (CBP). We inferred aspects of the genetic mating system of P. chihi in nature, using a genetic approach in the absence of parental information. We used five heterologous microsatellite loci and a multiple-step methodological approach to infer kinship patterns among 104 pairs of nestlings sampled inside 80 nests in a breeding colony from southern Brazil. The estimated effective population size was 69 white-faced ibises (95% CI: 50-98), enough to ensure long-term population survival. Kinship patterns were identified for 38% of the analyzed pairs: 60% of the diagnosed pairs were identified as full-siblings, 2.5% as half-siblings and 37.5% as unrelated individuals. CBP could explain the presence of unrelated nestlings within broods, in agreement with available non-genetic evidence. The presence of half-siblings within broods could indicate extra-pair paternity. Results suggest that a non-strictly monogamous genetic mating system may be present in the white-faced ibis. This study is the first molecular approach to better characterize the reproductive behavior of P. chihi in the wild. Our findings set the stage for further research to investigate the possible causes and consequences of alternative reproductive strategies in this species.

Colour Polymorphism and Alternative Breeding Strategies: Effects of Parent’s Colour Morph on Fitness Traits in the Common Wall Lizard

Colour polymorphism (CP) is widespread in animals, but mechanisms underlying morph evolution and maintenance are not completely resolved. In reptiles, CP is often genetically based and associated with alternative behavioural strategies, mainly in males for most cases. However, female colour morphs also display alternative reproductive strategies associated with behavioural and physiological traits, which may contribute to maintain CP in the population. Both sexes of the common wall lizard (Podarcis muralis) show three pure colour morphs, white, yellow and red. Here, we looked for the effects of male and female colour morphs on fitness traits of captive-breeding pairs. All yellow-throated females laid clutches of many small eggs and produced many light offspring, behaving as r-strategists, whereas white-throated females laid clutches of few large eggs and produced few heavy offspring, behaving as K-strategists. Red-throated females adopted a conditional Kr-strategy depending on their size/age. These basic female strategies were modulated in relation to mate morph: white females had the best fitness gain in terms of viable offspring when mated to red males; mating between yellow morphs yielded a greater breeding success than all other morph crosses, but also lighter offspring; finally, red females produced heavy progeny when paired with red or white males, and light offspring in pair with yellow males. Thus, correlation between CP and traits relevant to fitness combined with non-random mating, either assortative or disassortative, could increase the potential for CP to contribute to divergent evolution in the common wall lizard.

Transition to viviparity in the order Scorpaeniformes: Brief review

Among teleost percoid fishes (Percomorpha), the subordes Scorpaenoidei (Scorpaeniformes) and Zoarcoidei (Perciformes) are of particular interest due to the presence of intermediate stages between oviparity and viviparity in several species. We analyze the features of reproductive biology in the fishes of the suborder Scorpaenoidei, including morphology of the urogenital system, gametogenesis, gamete ultrastructure, and embryonic development. The new materials are represented for three tropical coral reef fish species with external insemination from the family Scorpaenidae (Scorpaenopsis possi, Sebastapistes cyanostigma, and Dendrochirus zebra). In particular, a hypertrophied urinary bladder used for storage of mature sperm for insemination of pelagic egg clutch is described in the males. Evolutionary transition to viviparity within the family Sebastidae is discussed. Alternative reproductive strategies are registered in viviparous fishes from the suborders Scorpaenoidei and Zoarcoidei. They are connected with the production of a large number of morphologically weakly developed larvae and a small number of individuals at the juvenile state, respectively.