The evolution of parental care in insects: the roles of ecology,life history and the social environment

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Sexual conflict in mammals: consequences for mating systems and life history

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Testing male immunocompetence in two hymenopterans with different levels of social organization: ‘live hard,die young?’

Males are under different selective pressures than females, which results in differences in the physiology of the two sexes to maximize their fitness. In terms of immunity, males are typically considered as the ‘sicker sex’, where immunocompetence is reduced to favour increased reproductive output. However, male social Hymenoptera are also haploid and therefore lack allelic variation at the individual level, which can also lead to reduced immunocompetence. Over the last decade, several studies have provided evidence for a higher susceptibility to disease in males of social Hymenoptera, without clarifying whether this susceptibility was a direct consequence of their haploid condition or the result of a ‘live hard, die young’ overall evolutionary strategy. In the present study, we used an experimental approach of bacterial challenge to test the immune response of males and females in two species of social Hymenoptera (honey bees, Apis mellifera; paper wasps, Polistes dominula), where males show very different life‐history traits. Drones benefit from colony protection for most of their life, whereas P. dominula males leave their colonies and have to survive for weeks at leks. If the haploid condition is responsible for a higher susceptibility in males, we should expect a lower immune response in males of both species compared to females. Conversely, if the immunocompetence depends on the life‐history traits of males, an opposite trend is expected in males of the two species. Our results do not support the ‘haploid susceptibility hypothesis’ but are in accordance with the different life history of males from the two species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 274–278.     

Patterns of hybridization in a multispecies hybrid zone in the Ranunculus cantoniensis complex (Ranunculaceae)

Simultaneous hybridizations among three or more parental taxa occur in nature, but these have rarely been analysed. The present study investigates the natural hybridization of diploid members of the Ranunculus cantoniensis complex over a microgeographical area in south‐western China. Sequence information from maternally inherited plastid DNA (trnQ‐rps16 and rpL32‐trnL) and biparentally inherited nuclear ribosomal DNA was used to identify hybrids, and these were further confirmed by a dramatic reduction in pollen viability. The populations from the contact zone contained individuals that had more than two nuclear ribosomal internal transcribed spacer (nrITS) types; in addition, a network analysis revealed the presence of hard conflicts between the nuclear and plastid DNA data. These results prove that R. trigonus and R. silerifolius var. dolicanthus have relatively little reproductive isolation from each other, leading to a high gene flow rate in contact populations. The four investigated species can hybridize with each other in this contact zone, forming seven hybrid types. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174 , 227–239.     

Snakes allocate amino acids acquired during vitellogenesis to offspring: are capital and income breeding consequences of variable foraging success?

Reproductive allocation strategies have been historically described as lying on a continuum between capital and income breeding. Capital breeders have been defined as species that allocate stored reserves to reproduction, whereas income breeders have been defined as species that allocate relatively recently‐ingested food resources to reproduction. Snakes are considered capital breeders because they efficiently store large amounts of nutrients and energy, potentially enough to support an entire reproductive bout without feeding. We examined the abilities of five viviparous snake species to allocate income to follicles during vitellogenesis. We fed ¹⁵N‐labelled L‐leucine to experimental females of each species during vitellogenesis, whereas control females were fed unlabelled meals. After ovulation, we measured yolk ¹⁵N p.p.m. using mass spectrometry. Maternal scale samples taken before labelling were used to estimate endogenous ¹⁵N concentrations, which should represent ‘capital’. Scale samples taken at ovulation were used to determine whether snakes assimilated ¹⁵N‐labelled‐leucine from labelled diets. Yolks and post‐ovulatory scales of labelled females were significantly more enriched in ¹⁵N than those of unlabelled females in all species, indicating significant assimilation and allocation of income‐derived amino acids to the yolk during vitellogenesis. The lack of among‐species differences suggests that all species allocated income amino acids to vitellogenesis. The results obtained in the present study suggest that proportional utilization of income or capital depends on the frequency and timing of foraging success during reproductive events. Therefore, capital and income breeding may be consequences of both life‐history and environmental constraints on foraging success, rather than strategies of reproductive allocation. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 390–404.     

Patterns of multiple paternity and maternity in fishes

The characterization of patterns of multiple mating is a major facet of molecular ecology and is paramount to understanding the evolution of behaviours associated with parental care and mate choice. Over the last 15 years, fishes have been particularly well studied with respect to multiple maternity and paternity thanks to the widespread application of microsatellite markers. The present review focusses on the impressive literature on genetic parentage in fishes. In studies of natural populations, we find that multiple paternity is extremely common across fish species, whereas rates of multiple maternity are much more variable. In species with nest defence, for example, rates of multiple maternity are strongly bimodal, and the occurrence of multiple dams per brood is either rare or the rule. The sex of the care‐giving parent is correlated with the rate of multiple parentage: when males provide uniparental care, rates of multiple paternity are low compared to rates of multiple maternity; when females provide parental care, either alone or assisted by males, rates of multiple paternity are highly variable, whereas rates of multiple maternity are quite low. These patterns may reflect conflicts between the reproductive interests of males and females. We also find that fishes in which females brood the offspring internally display much higher rates of multiple paternity compared to mammals or birds, whereas reptiles are intermediate. Male‐nesting fish species, however, show rates of multiple paternity more similar to those found in other vertebrates. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 735–760.     

Genetic population structure in prickly sculpin (Cottus asper) reflects isolation‐by‐environment between two life‐history ecotypes

Life‐history transitions have evolved repeatedly in numerous taxa, although the ecological and evolutionary conditions favouring such transitions in the presence of gene flow remain poorly understood. The present study aimed to disentangle the effects of isolation‐by‐distance and isolation‐by‐environment on genetic differentiation between two sympatric life‐history ecotypes. Using 14 microsatellite loci, we first characterized amphidromous and freshwater groups of Cottus asper in a high gene flow setting in the Lower Fraser River system (south‐western British Columbia, Canada) to test for the effects of habitat and geographical distance on the distribution of life‐history ecotypes. Within the main river channel, no genetic differentiation was found, whereas tributaries even close to the estuary were genetically differentiated. Partial mantel tests confirmed that genetic differentiation between river tributaries and the main channel was independent from geographical distance, with distance‐scaled migration rates indicating reduced gene flow from the main channel into the tributaries. Our results suggest that isolation‐by‐environment can play an important role for the early stage of life‐history transitions, and may promote differentiation among life‐history ecotypes despite the presence of gene flow. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 943–957.     

Reproductive biology and success of invasive Australian acacias in Portugal

Reproductive traits are crucial for the establishment and maintenance of populations in new areas, and therefore for the invasion process. This work aimed to study the reproductive biology of four aggressive invasive Australian Acacia spp. in Portugal. Fruit and seed set, seed weight and germinability, and seedling growth were assessed for self‐ and outcross treatments in invasive populations of A. dealbata, A. longifolia, A. melanoxylon and A. saligna. Acacia spp. showed different investments in the production of reproductive units and in natural reproductive success, with A. dealbata, the most aggressive species, having the highest investment and reproductive success. Acacia melanoxylon showed a different reproductive strategy, andromonoecy, contrasting with the other hermaphroditic species. Acacia spp. were shown to be predominantly self‐incompatible, but a low level of spontaneous selfing enabled the production of viable offspring. Acacia dealbata and A. longifolia suffered pollen limitation. Self‐progeny had lower viability than progeny from outcrossing for A. dealbata and A. melanoxylon. Acacia spp. did not show higher compatibility rates in comparison with the native area. They had low fruit set but, as a result of their massive flower production, their realized reproductive success was high and could have contributed to the invasion. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174 , 574–588.     

Development and the effects of extended parenting in the cold‐breeding burying beetle Nicrophorus sayi

1. Burying beetles (Nicrophorus spp.) provide an excellent model system to test predictions about the relationships between environment, life‐history and behaviour. All species in the genus display similar natural histories, breeding on vertebrate carcasses and providing parental care to developing offspring. However, variations in other aspects of species' ecologies provide a rich framework to examine the evolution of parental behaviours and other traits. 2. One little‐studied species, N. sayi, breeds in substantially colder temperatures than its congeners, creating a potentially harsh environment for offspring. Here, we examined the timing of reproductive and developmental events in this species, and also investigated the effects of removing parents on offspring performance. 3. We find that development is not only extremely slow in this species, but it is also delayed even in comparison to other burying beetles reared at similar temperatures. However, the presence of parents reduces the time that offspring take to leave the carcass. This decrease in development time does not appear to result in a trade‐off with mortality or body size. 4. From these results, we suggest that very slow development may be advantageous when living in a particularly cold environment. Additionally, one role of extended parental care may be to assist offspring in dealing with these harsh conditions, and to mitigate the potentially negative consequences of adopting such a slow life‐history strategy.     

Genetic and morphologic diversity of European fan palm (Chamaerops humilis L.) populations from different environments from Sicily

Chamaerops humilis is decreasing in abundance in Mediterranean Europe, which has induced the European community to call for its protection in Special Areas of Conservation. However, information about its genetic and morphological variability, which is crucial to the development of any conservation strategies, is insufficient. The present study aimed to investigate the genetic and morphological variability of C. humilis in Sicily, which was selected as a model because of the high number of dense populations. The relationships between morphological traits and climatic variables were studied to highlight patterns of adaptation to the environment, along with the genetic similarity among the populations. Ten natural populations were sampled, analyzed using 28 specifically designed SSR primers, and evaluated based on 29 morphological traits. The populations were clustered similarly based on genetic and morphological traits. Heterozygosity was high and inbreeding coefficients were low. These results, along with higher intra‐ than inter‐population differentiation, suggest that C. humilis populations in Sicily differentiated from a common ancestor and that inter‐population variation arose from secondary evolution processes induced by ecological adaptation. The correlations between climatic variables and morphological traits suggest that the morphological adaptation to arid environments depends more on summer temperatures than on evapotranspiration or rainfall and that autumn and winter temperatures are determinants of the species establishment at new sites. Considering the response of C. humilis to seasonal temperatures, the present results indicate this species as a candidate for tracking climatic changes in Europe. Further studies are needed to highlight the adaptation of C. humilis to cold environments. Palaeo‐climatological and ‐ecological studies could help clarify its strategies for the colonization of new sites. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 176 , 66–81.     

Ontogeny of the proliferous spikelet in Eleocharis 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. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 176 , 524–539.     

The effectiveness of pre‐ and post‐zygotic barriers in avoiding hybridization between two snapdragons (Antirrhinum L.: Plantaginaceae)

Reproductive barriers play an important role in the maintenance of species boundaries. However, to date, few studies have provided a detailed analysis of reproductive isolation barriers between species or examined their importance in maintaining species identity. This is the first detailed study into pre‐ and post‐zygotic reproductive isolation barriers in Antirrhinum, based on a mixed population with two species that rarely co‐occur. The study revealed that pollinator constancy and preference and poor hybrid seed viability were the most important reproductive isolating mechanisms. Reproductive isolation was practically complete by both pre‐ and post‐zygotic barriers. Average pre‐zygotic isolation was greater than post‐zygotic isolation, in accordance with the trend observed in flowering plants in which reproductive isolation is principally caused by pre‐zygotic mechanisms. However, average post‐zygotic isolation was also high, in contrast to what was expected among Antirrhinum spp. This case highlights the importance of quantifying the reproductive isolation barriers thoroughly to understand how and why species boundaries are maintained. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 176 , 159–172.     

Patterns and drivers of intraspecific variation in avian life history along elevational gradients: a meta‐analysis

Elevational gradients provide powerful natural systems for testing hypotheses regarding the role of environmental variation in the evolution of life‐history strategies. Case studies have revealed shifts towards slower life histories in organisms living at high elevations yet no synthetic analyses exist of elevational variation in life‐history traits for major vertebrate clades. We examined (i) how life‐history traits change with elevation in paired populations of bird species worldwide, and (ii) which biotic and abiotic factors drive elevational shifts in life history. Using three analytical methods, we found that fecundity declined at higher elevations due to smaller clutches and fewer reproductive attempts per year. By contrast, elevational differences in traits associated with parental investment or survival varied among studies. High‐elevation populations had shorter and later breeding seasons, but longer developmental periods implying that temporal constraints contribute to reduced fecundity. Analyses of clutch size data, the trait for which we had the largest number of population comparisons, indicated no evidence that phylogenetic history constrained species‐level plasticity in trait variation associated with elevational gradients. The magnitude of elevational shifts in life‐history traits were largely unrelated to geographic (altitude, latitude), intrinsic (body mass, migratory status), or habitat covariates. Meta‐population structure, methodological issues associated with estimating survival, or processes shaping range boundaries could potentially explain the nature of elevational shifts in life‐history traits evident in this data set. We identify a new risk factor for montane populations in changing climates: low fecundity will result in lower reproductive potential to recover from perturbations, especially as fewer than half of the species experienced higher survival at higher elevations.     

Reproductive ecology of female caecilian amphibians (genus Ichthyophis): a baseline study

The remarkable diversity of reproductive modes, including levels of parental care that are extensive relative to those of the other major amphibian groups, makes the limbless tropical caecilians ideally suited for evolutionary reproductive studies. Here we present key life history data for the oviparous caecilian Ichthyophis cf. kohtaoensis. We used non-invasive methods to analyse reproductive traits, seasonality of breeding and characteristics of oviposition sites in the field (Mekong valley, north-eastern Thailand). A correlation was established between reproductive activity and season, indicated by the age of egg clutches found in the field. Eggs at early developmental stages were found at the beginning of the rainy season, those with well-developed embryos at the peak of the monsoon. The body condition of females guarding younger clutches was superior to that of females with older clutches, indicative of a loss of energy reserves during the period of parental care. Maternal total length correlated positively with the number of eggs as well as with the total length of newly hatched larvae. The terrestrial oviposition sites of females were located close to temporary and permanent ponds, small brooks and rivers. It is hoped that the study will, in addition to contributing to our understanding of the evolution of caecilian reproduction, provide a basis for further comparisons of reproductive strategies among amphibians and other terrestrial tetrapods.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 207–217.     

Population differentiation and speciation in the genus Characidium (Characiformes: Crenuchidae): effects of reproductive and chromosomal barriers

Both time and low gene flow are the key factors by which different biological species arise. The divergence process among lineages and the development of pre‐ or postzygotic isolation occur when gene flow events are lacking. The separation among species of the genus Characidium was analysed in relation to the geomorphological mechanisms in river courses, events of captured adjacent upland drainages in south‐eastern Brazil, and sex chromosome differences. The ZZ/ZW sex chromosomes of Characidium vary in size, morphology, degree of heterochromatinization, and presence/absence of ribosomal DNA. The goal of this study was to understand the mechanism of sex chromosome differentiation, its close association with the geological history of cladogenetic events among drainages, and reproductive isolation leading to Characidium speciation. The W‐specific probe from Characidium gomesi generated a highlighted signal on the entire W chromosome of C. gomesi, Characidium heirmostigmata, Characidium pterostictum, and Characidium sp., instead of karyotypes of three Characidium aff. zebra populations, which showed scattered signals. An evolutionary and biogeographic landscape arose by analysis of ribosomal DNA site location and differentiation of the sex chromosomes, which established mechanisms of reproductive isolation leading to meiotic barriers, keeping the biological unit distinct even if the contact among species was restored. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 541–553.     

A comparison of life‐history and parental care in temperate and tropical wrens

Comparing closely related species that live in different environments is a powerful way to understand selective pressures that influence life‐history evolution. We examined a suite of life‐history traits and parental care in neotropical buff‐breasted wrens Cantorchilus leucotis and north‐temperate Carolina wrens Thryothorus ludovicianus (Family Troglodytidae), to test hypotheses about life‐history evolution. As expected, buff‐breasted wrens exhibited smaller clutch sizes and higher annual adult survival than Carolina wrens. We found minimal support for the nest predation hypothesis, as nest survival and age‐corrected provisioning rates to whole broods were similar between species, and number of breeding attempts and breeding season length were greater in temperate wrens. Critical predictions of the food limitation hypothesis were not supported; in particular age‐corrected provisioning rates per nestling were higher in the tropical than temperate species. The adult survival and offspring quality hypothesis garnered the most support, as buff‐breasted wrens exhibited greater age‐corrected provisioning rates per nestling, a longer nestling period, longer re‐nesting intervals following nest success, and lower annual fecundity than Carolina wrens. Despite similarly prolonged breeding seasons, reproductive strategies differ between species with buff‐breasted wrens investing considerably in single broods to optimize first‐year survival and Carolina wrens investing in multiple small broods to optimize annual fecundity.     

Populations composed entirely of hybrid colonies: bidirectional hybridization and polyandry in harvester ants

In eusocial Hymenoptera, haplodiploid life cycles, obligate sterile castes, and polyandry may facilitate selection for hybridization. We analyzed a broad hybrid zone between the ecologically distinct seed‐harvester ants Pogonomyrmex occidentalis (Cresson) and Pogonomyrmex maricopa (Wheeler) using mitochondrial (mt)DNA sequence data, eight morphological markers, and 14 random amplified polymorphic DNA (RAPD) markers. Average mtDNA sequence divergence among parental species was 11.34%, indicating secondary contact. RAPD markers were significantly correlated with morphological variation, confirming the interspecific hybrid origin of all morphologically putative hybrid colonies. A morphological hybrid index indicates an abundance of both F₁ hybrids and parental morphotypes within colonies. Individual character frequencies plotted against distance show coincident and concordant clines, suggesting little to no introgression. The structure of the hybrid zone is two‐fold. Within the western region, stark reversals in character frequencies coincide with overt soil differences, indicating a mosaic hybrid zone structure. The eastern region is a riparian habitat where four adjacent populations were composed entirely of hybrid colonies. These habitat associations suggest that hybrid worker genomes permit dispersal into intermediate environments that select against one or both parental species. The present study suggests that, in addition to retaining reproductive compatibility, ecologically distinct species of ants may generate hybrid colonies maintained by environmental selection. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 320–336.     

A review of the ecological parameters and implications of subsociality in Parastrachia japonensis (Hemiptera: Cydnidae), a semelparous species that specializes on a poor resource

Subsocial behavior or postovipositional parental care in insects has evolved in response to a variety of environmental stresses and ranges from briefly guarding eggs after oviposition to elaborate nidification and provisioning behaviors. Investment in parental care bears various costs, and should not continue beyond the point at which the costs to future reproductive success exceed the benefits to current reproductive effort. Progressive provisioning is a rare form of subsociality in insects. Females of the subsocial shield bug Parastrachia japonensis progressively provision their nymph-containing nests with drupes of the single resource, Schoepfia jasminodora, and this provisioning drastically enhances offspring survival. A female rears only one brood throughout her lifetime and continues provisioning the brood until about the third larval stadium, when the female dies. Thus, the female's entire reproductive effort is expressed in the success of that one brood, which suggests a reproductive strategy with enormous costs and risks. Why has such an extreme life history evolved in this species? Here, to answer that question and to contribute to our understanding of the evolutionary implications of subsocial behavior, in particular, progressive provisioning, we review what we have discovered about the ecological parameters of subsociality in this species during a long-term field study. We also discuss these parameters in P. japonensis in reference to other subsocial insects and related species and conclude with a suggestion that semelparity and progressive provisioning in this species are extreme adaptations to evolving complete dependency on an unreliable resource.     

Extra-pair paternity and egg dumping in birds: life history,parental care and the risk of retaliation

Molecular techniques have revealed striking variation among bird species in the rates of extra-pair paternity (EPP) and intraspecific brood parasitism (IBP). In terms of the proportion of broods affected, rates of EPP and IBP vary across species from 0-95% and 0-50%, respectively. Despite a plethora of hypotheses and several careful comparative analyses, few robust correlates of this interspecific variation have been identified. One explanation for this shortfall is that most comparative studies have tended to focus on contemporary ecological factors and ignored fundamental differences in reproductive biology that evolved millions of years ago. We show that, for both EPP and IBP, over 50% of interspecific variation is due to differences among taxonomic families and orders. Therefore, we test hypotheses that predict interspecific variation in the rate of alternative reproductive strategies should be associated with differences in life history and the form of parental care. Our analyses largely support these predictions, with high rates of reproductive cheating being associated with 'fast' life histories. High EPP rates are associated with high rates of adult mortality and reduced paternal care. High IBP rates are associated with high-fecundity rates. These patterns remain intact whether we use species as independent data points or evolutionary contrasts based on either molecular or morphological phylogenies. These results are interpreted as supporting the idea that alternative reproductive strategies are most common in taxa in which the risks of retaliation are low. We suggest a hierarchical explanation for interspecific variation in the incidence of alternative reproductive strategies. Variation between major avian lineages in the EPP and IBP rates are determined by fundamental differences in life history and parental care that evolved many millions of years ago. Variation between populations or individuals of the same species, however, are more likely to be determined by differences in contemporary ecological and genetic factors.