Evolution Of Breeding Systems Research Articles

First detailed report of cooperative breeding in red-billed blue magpie (Urocissa erythrorhyncha) in central China

Abstract The cooperative breeding system of birds is an ideal model for studying and exploring social evolution in animals. However, a basic question, i.e., how many cooperative-breeding bird species exist in the world, remains controversial due to the lack of accumulated knowledge of the natural history of many birds, which prevents a generalized understanding of the evolution of cooperative breeding in birds and challenges the accuracy of results in many comparative studies. In this paper, we provide the first evidence of cooperative breeding in red-billed blue magpies (Urocissa erythrorhyncha). Moreover, we document and discuss potential relationships between cooperative breeding and nest predation, brood parasitism and breeding performance in U. erythrorhyncha. These findings about cooperative breeding in red-billed blue magpie will lay a foundation for further research on this species’ sociality and provide useful insights into the evolution of cooperative breeding and other social systems in birds.

Systematic revision of the ‘diminutive’ Kentish Plover (Charadriidae: Charadrius) with the resurrection of Charadrius seebohmi based on phenotypic and genetic analyses

The Kentish Plover Charadrius alexandrinus Linnaeus 1758 is a common shorebird in Eurasia and North Africa that breeds in a variety of habitats, exhibits different extents of migratory behaviour and is an emerging model species of breeding system evolution. Here we focus on the resident population found across the southern tip of India and Sri Lanka, and re‐evaluate its systematic status based on phenotypic and genetic distinctiveness from a sympatric migrant, Charadrius alexandrinus sensu stricto, and the recently elevated closely related Charadrius dealbatus in East Asia. We show that the Sri Lankan and South Indian (South Asian) population differs in body size, moulting pattern and plumage coloration from C. alexandrinus and C. dealbatus. Furthermore, based on two mitochondrial, two sex‐linked and 11 autosomal microsatellite markers from 378 individuals, we show that these three taxa have moderate genetic differentiation (Fst 0.078–0.096). The South Asian taxon is sister to the clade of C. alexandrinus sensu stricto and C. dealbatus with an estimated divergence time of 1.19 million years ago. We also examined ornithological records of major museum collections in Asia, Europe and North America for the south Asian taxon to evaluate its biogeographical and taxonomic status. Based on differences in genotype, phenotype, allochronic migratory pattern and breeding range, we resurrect the most suitable synonym, Charadrius alexandrinus seebohmi Hartert and Jackson, 1915, and elevate the nomen to the species level with the proposed English name ‘Hanuman Plover’.

Colonial breeding birds show greater annual adult apparent survival globally

Colonial breeding is a common breeding system in many avian species. Its ubiquity suggests that in the evolutionary past various benefits associated with colonial breeding often outweighed the potential costs. I have investigated the association between one fitness component, namely annual adult survival, and colonial breeding. Using a global dataset of survival probabilities (2431 survival estimates from 1170 species including 213 colonial species), I found that annual adult apparent survival was greater in colonial than in solitary breeding species in both hemispheres after including phylogeny and considering potential ecological confounders such as body mass and latitude. Excluding Procellariiformes, a clade of birds with unique features (all marine colonial species laying single‐egg clutches), did not alter the conclusions. This was also the case when excluding species living year‐long on islands, which are typically non‐colonial and long‐lived, and when excluding studies where survival estimates did not account for recapture/resighting probabilities, which might differ according to breeding system. Greater annual adult apparent survival is therefore a robust feature of colonial breeding in birds, which sheds light on the evolution of this common breeding system. Future studies are needed across species to determine whether the survival advantage of colonial breeding extends to nestlings and juveniles.

Unique arrangement and temporal separation of essential organs promotes cross pollination in Impatiens edgeworthii Hook. f.: an endemic species of Western Himalaya

Impatiens edgeworthii is an important plant species endemic to Western Himalaya. In this species male reproductive organs conceal the stigma – seat of pollen reception during male phase therefore acts as barrier for self-pollination. In addition the stigma become receptive only after the androecium of the same flower is shed and then receptive stigma become exposed. This unique type of dichogamy and arrangement of essential organs are contrivance for cross-pollination in the species. The large showy flowers, production of large quantities of nectar, protandry, presence of nectar guides, ornamented exine sculpturing, high pollen to ovule ratio points towards cross-pollinated mode of reproduction is operative in this species. This was also established by breeding experiments. Our study may prove useful in conservation of this Himalayan endemic plant species and also useful in understanding the evolution of breeding system in the genus.

Long-read transcriptome and other genomic resources for the angiosperm Silene noctiflora.

The angiosperm genus Silene is a model system for several traits of ecological and evolutionary significance in plants, including breeding system and sex chromosome evolution, host-pathogen interactions, invasive species biology, heavy metal tolerance, and cytonuclear interactions. Despite its importance, genomic resources for this large genus of approximately 850 species are scarce, with only one published whole-genome sequence (from the dioecious species Silene latifolia). Here, we provide genomic and transcriptomic resources for a hermaphroditic representative of this genus (S. noctiflora), including a PacBio Iso-Seq transcriptome, which uses long-read, single-molecule sequencing technology to analyze full-length mRNA transcripts. Using these data, we have assembled and annotated high-quality full-length cDNA sequences for approximately 14,126 S. noctiflora genes and 25,317 isoforms. We demonstrated the utility of these data to distinguish between recent and highly similar gene duplicates by identifying novel paralogous genes in an essential protease complex. Furthermore, we provide a draft assembly for the approximately 2.7-Gb genome of this species, which is near the upper range of genome-size values reported for diploids in this genus and threefold larger than the 0.9-Gb genome of Silene conica, another species in the same subgenus. Karyotyping confirmed that S. noctiflora is a diploid, indicating that its large genome size is not due to polyploidization. These resources should facilitate further study and development of this genus as a model in plant ecology and evolution.

Resolved phylogenetic relationships in the Ocotea complex (Supraocotea) facilitate phylogenetic classification and studies of character evolution.

The Ocotea complex contains the greatest diversity of Lauraceae in the Neotropics. However, the traditional taxonomy of the group has relied on only three main floral characters, and previous molecular analyses have used only a few markers and provided limited support for relationships among the major clades. This lack of useful data has hindered the development of a comprehensive classification, as well as studies of character evolution. We used RAD-seq data to infer the phylogenetic relationships of 149 species in the Ocotea complex, generating a reference-based assembly using the Persea americana genome. The results provide the basis for a phylogenetic classification that reflects our current molecular knowledge and for analyses of the evolution of breeding system, stamen number, and number of anther locules. We recovered a well-supported tree that demonstrates the paraphyly of Licaria, Aniba, and Ocotea and clarifies the relationships of Umbellularia, Phyllostemonodaphne, and the Old World species. To begin the development of a new classification and to facilitate precise communication, we also provide phylogenetic definitions for seven major clades. Our ancestral reconstructions show multiple origins for the three floral characters that have routinely been used in Lauraceae systematics, suggesting that these be used with caution in the future. This study advances our understanding of phylogenetic relationships and character evolution in a taxonomically difficult group using RAD-seq data. Our new phylogenetic names will facilitate unambiguous communication as studies of the Ocotea complex progress.

The Organization for Tropical Studies: History, accomplishments, future directions in education and research, with an emphasis in the contributions to the study of plant reproductive ecology and genetics in tropical ecosystems

The Organization for Tropical Studies (OTS) has played a pivotal role in our understanding of tropical ecosystems' structure and function. For more than fifty years, OTS has contributed to the training of three generations of tropical biologists and facilitated, supported, and promoted leading-edge research in its field stations. Plant reproductive ecology and genetics have been a significant focus of OTS research since the early 1960s, and Dr. K.S. Bawa made a significant contribution to the advancement of this field. His work improved our understanding of the diversity and evolution of breeding systems in tropical forests, their phenology and pollination ecology, and their mating and genetic structure. We argue that his work inspired other tropical biologists' work and used the work of one of the authors for illustration when appropriate. We point out the need for research in critically important topics to slow down biodiversity loss, prevent the collapse of tropical systems in a changing climate, and the emergence of zoonotic disease. We suggest future research topics for the OTS field stations, including in plant reproductive biology.

The de novo genome assembly of Tapiscia sinensis and the transcriptomic and developmental bases of androdioecy

Tapiscia sinensis (Tapisciaceae) possesses an unusual androdioecious breeding system that has attracted considerable interest from evolutionary biologists. Key aspects of T. sinensis biology, including its biogeography, genomics, and sex-linked genes, are unknown. Here, we report the first de novo assembly of the genome of T. sinensis. The genome size was 410 Mb, with 22,251 predicted genes. Based on whole-genome resequencing of 55 trees from 10 locations, an analysis of population genetic structure indicated that T. sinensis has fragmented into five lineages, with low intrapopulation genetic diversity and little gene flow among populations. By comparing whole-genome scans of male versus hermaphroditic pools, we identified 303 candidate sex-linked genes, 79 of which (25.9%) were located on scaffold 25. A 24-kb region was absent in hermaphroditic individuals, and five genes in that region, TsF-box4, TsF-box10, TsF-box13, TsSUT1, and TsSUT4, showed expression differences between mature male and hermaphroditic flowers. The results of this study shed light on the breeding system evolution and conservation genetics of the Tapisciaceae.

Testing Weissman's Lineage Selection Model for the Maintenance of Sex: The Evolutionary Dynamics of Clam Shrimp Reproduction over Geologic Time.

One of the most perplexing questions within evolutionary biology is: "why are there so many methods of reproduction?" Contemporary theories assume that sexual reproduction should allow long term survival as dispersal and recombination of genetic material provides a population of organisms with the ability to adapt to environmental change. One of the most frustrating aspects of studying the evolution of reproductive systems is that we have not yet been able to utilize information locked within the fossil record to assess breeding system evolution in deep time. While the fossil record provides us with information on an organism's living environment, as well as some aspects of its ecology, the preservation of biological interactions (reproduction, feeding, symbiosis, communication) is exceedingly rare. Using both information from extant taxa uncovered by a plethora of biological and ecological studies and the rich representation of the Spinicaudata (Branchiopoda: Crustacea) throughout the fossil record (from the Devonian to today), we address two hypotheses of reproductive evolutionary theory: (1) that unisexual species should be short lived and less speciose than their outcrossing counterparts and (2) that androdioecy (mixtures of males and hermaphrodites) is an unstable, transitionary system that should not persist over long periods of time. We find no evidence of all-unisexual spinicaudatan taxa (clam shrimp) in the fossil record, but do find evidence of both androdioecious and dioecious clam shrimp. We find that clades with many androdioecious species are less speciose but persist longer than their mostly dioecious counterparts. These data suggest that all-unisexual lineages likely do not persist long whereas mixtures of unisexual and sexual breeding can persist for evolutionarily long periods but tend to produce fewer species than mostly sexual breeding.

Kin-dependent dispersal influences relatedness and genetic structuring in a lek system.

Kin selection and dispersal play a critical role in the evolution of cooperative breeding systems. Limited dispersal increases relatedness in spatially structured populations (population viscosity), with the result that neighbours tend to be genealogical relatives. Yet the increase in neighbours' fitness-related performance through altruistic interaction may also result in habitat saturation and thus exacerbate local competition between kin. Our goal was to detect the footprint of kin selection and competition by examining the spatial structure of relatedness and by comparing non-effective and effective dispersal in a population of a lekking bird, Tetrao urogallus. For this purpose, we analysed capture-recapture and genetic data collected over a 6-year period on a spatially structured population of T. urogallus in France. Our findings revealed a strong spatial structure of relatedness in males. They also indicated that the population viscosity could allow male cooperation through two non-exclusive mechanisms. First, at their first lek attendance, males aggregate in a lek composed of relatives. Second, the distance corresponding to non-effective dispersal dramatically outweighed effective dispersal distance, which suggests that dispersers incur high post-settlement costs. These two mechanisms result in strong population genetic structuring in males. In females, our findings revealed a lower level of spatial structure of relatedness and genetic structure in respect to males. Additionally, non-effective dispersal and effective dispersal distances in females were highly similar, which suggests limited post-settlement costs. These results indicate that kin-dependent dispersal decisions and costs have a genetic footprint in wild populations and are factors that may be involved in the evolution of cooperative courtship.

Home range overlap and its genetic correlates in an avian brood parasite, the lesser cuckoo Cuculus poliocephalus

The absence of parental care is of importance in the evolution of mating and breeding systems. However, its importance in the evolution of these systems in higher vertebrates, such as birds and mammals, has not been well defined since nearly all of them exhibit some form of parental care. Avian brood parasites thus provide a unique opportunity to explore the effect of a lack of parental care in higher vertebrates because they shift care for their progeny onto other species. We investigated the social system of an avian brood parasite, the lesser cuckoo (Cuculus poliocephalus), by using a comprehensive approach that included field observation, radio-tracking, and genetic analyses. We found that genetically unrelated, multiple males and females coexist in a single area; radio-tracking confirmed that this co-occurrence was neither temporary nor arbitrary. Instead, sympatric cuckoos appeared to share their home ranges and often chased each other for mating without antagonistic physical interaction. We conclude that the lesser cuckoo may employ a scramble competition mating system without territoriality, and that this mating system, which is unusual in higher vertebrates, may have arisen due to the absence of parental care. Future studies assessing the parentage of nestlings are needed to establish the genetic basis of this social system.

Genome Evolution in Outcrossing vs. Selfing vs. Asexual Species.

A major current molecular evolution challenge is to link comparative genomic patterns to species' biology and ecology. Breeding systems are pivotal because they affect many population genetic processes and thus genome evolution. We review theoretical predictions and empirical evidence about molecular evolutionary processes under three distinct breeding systems-outcrossing, selfing, and asexuality. Breeding systems may have a profound impact on genome evolution, including molecular evolutionary rates, base composition, genomic conflict, and possibly genome size. We present and discuss the similarities and differences between the effects of selfing and clonality. In reverse, comparative and population genomic data and approaches help revisiting old questions on the long-term evolution of breeding systems.

Floral polymorphism in <i>Polygonum bistorta</i> L.

In the present study, new type of floral polymorphism (tristylous-like flowers) in Polygonum bistorta L., i.e., L-, M-, and S-styles (long, medium and short, respectively) is reported. This tristylous was not only present in different populations but also in a single inflorescence. Although the heights of styles and anthers in the three morphs of flowers differed, their ancillary tepal size, pollen polymorphism, and stigma polymorphism were found similar. The ratio of M-flowers was far lower than those of L- and S-flowers. Unlike the solid nectar of other Polygonum species, fluid nectar was present in Polygonum bistorta, which reflects its specialized state. Different from most of other hetereostylous species with tubular flowers and Polygonum jucundum with open distylous flowers, Polygonum bistorta contains semi-open flowers. Our findings suggest that P. bistorta represents special floral polymorphism in Polygonum and is an ideal plant species for studying the evolution of floral breeding system in Polygonum.Bangladesh J. Plant Taxon. 25(1): 1-11, 2018 (June)

Estimating divergence times and ancestral breeding systems in Ficus and Moraceae.

Although dioecy, which characterizes only 6 % of angiosperm species, has been considered an evolutionary dead end, recent studies have demonstrated that this is not necessarily the case. Moraceae (40 genera, 1100 spp., including Ficus, 750 spp.) are particularly diverse in breeding systems (including monoecy, gynodioecy, androdioecy and dioecy) and thus represent a model clade to study macroevolution of dioecy. Ancestral breeding systems of Ficus and Moraceae were inferred. To do so, a new dated phylogenetic tree of Ficus and Moraceae was first reconstructed by combining a revised 12-fossil calibration set and a densely sampled molecular data set of eight markers and 320 species. Breeding system evolution was then reconstructed using both parsimony and model-based (maximum likelihood and Bayesian) approaches with this new time scale. The crown group ages of Ficus and Moraceae were estimated in the Eocene (40.6-55.9 Ma) and Late Cretaceous (73.2-84.7 Ma), respectively. Strong support was found for ancestral dioecy in Moraceae. Although the ancestral state of Ficus remained particularly sensitive to model selection, the results show that monoecy and gynodioecy evolved from dioecy in Moraceae, and suggest that gynodioecy probably evolved from monoecy in Ficus. Dioecy was found not to be an evolutionary dead end in Moraceae. This study provides a new time scale for the phylogeny and a new framework of breeding system evolution in Ficus and Moraceae.

Breeding system and pollination of Gesneria pauciflora (Gesneriaceae), a threatened Caribbean species

Knowledge of plant breeding systems may be critical to facilitate recovery of species considered at risk. Gesneria pauciflora is a threatened, rupiculous, and riverine species with floral-traits that suggest a hummingbird-pollination system. Because these habitat-pollinator conditions have been linked to pollinator-independent reproductive systems, we expected a breeding system that provides reproductive assurance. We assessed the breeding system and potential vulnerabilities during pollination phase using field observations and pollination experiments, to determine pollinator dependency and the existence of strategies for reproductive assurance. Gesneria pauciflora was pollinated by two hummingbird species but visitation rates were low, probably due to low nectar rewards. Fruit set and seed production were significantly higher in flowers when pollen was artificially delivered (self- and cross-pollination) compared to when it was not (control and autogamy), suggesting that reproduction is pollen-limited. Gesneria pauciflora is self-compatible, with some seeds produced via autonomous selfing without any effects of pollination mechanism on seed germination rates. Florivory by the native plume-moth Postplatyptilia caribica was observed, but its incidence was low (12%). Our findings are consistent with theory on the evolution of plant breeding systems on islands, and contribute to the understanding of the evolution of breeding systems in Caribbean gesneriads. Overall, data do not show immediate vulnerabilities to this listed species at the pollination phase, and autogamy may represent reproductive assurance counteracting unpredictable environmental factors that influence its reproduction. However, its capacity for selfing is small relative to other tubular Puerto Rican Gesneria which may explain its rare status.

Preadaptation for asexual queen succession: queen tychoparthenogenesis produces neotenic queens in the termite Reticulitermes okinawanus

Social insects have evolved diverse breeding systems. In the termite species Reticulitermes speratus, queens produce their neotenic replacements parthenogenetically while producing other colony members sexually. This asexual queen succession (AQS) system enables the colony to undergo queen succession and increase the number of queens while avoiding king–daughter inbreeding, which must otherwise result in loss of genetic diversity in the workforce. The evolution of this sophisticated breeding system requires both parthenogenetic ability and parthenogens’ developmental priority to become neotenic queens. However, the evolutionary process of these two components is unknown. In this study, we investigated the caste fate of the offspring produced by tychoparthenogenesis in a non-AQS termite species Reticulitermes okinawanus. The hatching rate of unfertilized eggs in R. okinawanus (0.97%) was much lower than that in the AQS species R. speratus (75%). Flow cytometry and genetic analyses were used to demonstrate that R. okinawanus tychoparthenogenesis produced diploid homozygous females. One-third of the daughters from unfertilized eggs developed into neotenics, while no sexually produced daughters differentiated into neotenics. These results suggest that parthenogenetic daughters have the developmental propensity to become neotenic queens prior to the inception of AQS.

Outbreeding depression and breeding system evolution in small, remnant populations of Primula vulgaris: consequences for genetic rescue

Many species suffer from anthropogenic habitat fragmentation. The resulting small and isolated populations are more prone to extinction due to, amongst others, genetic erosion, inbreeding depression and Allee-effects. Genetic rescue can help mitigate such problems, but might result in outbreeding depression. We evaluated offspring fitness after selfing and outcrossing within and among three very small and isolated remnant populations of the heterostylous plant Primula vulgaris. We used greenhouse-grown offspring from these populations to test several fitness components. One population was fixed for the pin-morph, and was outcrossed with another population in the field to obtain seeds. Genetic diversity of parent and offspring populations was studied using microsatellites. Morph and population-specific heterosis, inbreeding and outbreeding depression were observed for fruit and seed set, seed weight and cumulative fitness. Highest fitness was observed in the field-outcrossed F1-population, which also showed outbreeding depression following subsequent between-population (back)crossing. Despite outbreeding depression, fitness was still relatively high. Inbreeding coefficients indicated that the offspring were more inbred than their parent populations. Offspring heterozygosity and inbreeding coefficients correlated with observed fitness. One population is evolving homostyly, showing a thrum morph with an elongated style and high autonomous fruit and seed set. This has important implications for conservation strategies such as genetic rescue, as the mating system will be altered by the introduction of homostyles.

Pollination context alters female advantage in gynodioecious Silene vulgaris.

Gynodioecy, the co-occurrence of females and hermaphrodites, is arguably the most common angiosperm gender polymorphism in many florae. Females' ability to invade and persist among hermaphrodites depends, in part, on pollinators providing adequate pollination to females. We directly measured diurnal and nocturnal pollinators' contributions to female and hermaphrodite seed production in artificial populations of gynodioecious Silene vulgaris by experimentally restricting pollinator access. We found that female relative seed production in this system depended strongly on pollination context: females produced more than twice as many seeds as hermaphrodites in the context of abundant, nectar-collecting moths. Conversely, females showed no seed production advantage in the context of pollen-collecting syrphid flies and bees due to acutely hermaphrodite-biased visitation. We infer that variation in pollinator type, behaviour and abundance may be important for achieving the female relative fitness thresholds necessary for the maintenance of gynodioecy. Generally, our study illustrates how pollinator-mediated mechanisms may influence the evolution of breeding systems and associated suites of floral traits. Segments of a pollinator community may facilitate gynodioecy by selecting for plant characteristics that increase the attractiveness of both sexes to pollinators, such as nectar rewards. Conversely, discriminating visitors in search of pollen may restrict gynodioecy in associated plant lineages by reducing male steriles' fitness below threshold levels.

Dioecious plants are more precocious than cosexual plants: A comparative study of relative sizes at the onset of sexual reproduction in woody species.

The reproductive capacities of dioecious plant species may be limited by severe pollen limitation and narrow seed shadows for the two reasons. First, they are unable to self‐pollinate, and seed production occurs only with pollinator movement from males to females. Second, only 50% of the individuals in populations contribute to seed production. Despite these handicaps, dioecious plants maintain their populations in plant communities with cooccurring cosexual plants, and no substantial difference in population growth rates has been found between dioecious and cosexual plants. Hence, dioecious plants are thought to mitigate these disadvantages by adopting ecological traits, such as insect pollination, animal‐dispersed fleshy fruits, and precocious flowering. We studied the relationship between flowering and plant size in 30 woody species with different sex expressions, leaf habits, fruit types, and maximum plant sizes. The study site was located in an evergreen broad‐leaved forest on the island of Honshu, Japan. A phylogenetic linear regression model showed that dioecious species tended to mature at smaller sizes than did cosexual taxa. At the population level, given equal plant densities and reproductive efforts, the precocity of dioecious plants could serve as one of the factors that mitigate the limitations of pollen and seed‐shadow handicaps by increasing the density of reproductive individuals in the population. At the individual level, smaller size of onset of flowering may play a role in enhancing reproductive success over a lifetime by increasing reproductive opportunities. We discussed the possible effect of the relationship between precocity and some ecological traits of dioecious plants, such as small flowers pollinated by unspecialized insects, fleshy fruit dispersed by animals, and their preferential occurrence in the tropics and in island habitats. The universality of precocity among dioecious plants should be investigated in diverse plant communities. Such studies will increase our understanding of the evolution of plant breeding systems.

Sex‐biased oviposition by a nursery pollinator on a gynodioecious host plant: Implications for breeding system evolution and evolution of mutualism

Dioecy, a breeding system where individual plants are exclusively male or female, has evolved repeatedly. Extensive theory describes when dioecy should arise from hermaphroditism, frequently through gynodioecy, where females and hermaphrodites coexist, and when gynodioecy should be stable. Both pollinators and herbivores often prefer the pollen‐bearing sex, with sex‐specific fitness effects that can affect breeding system evolution. Nursery pollination, where adult insects pollinate flowers but their larvae feed on plant reproductive tissues, is a model for understanding mutualism evolution but could also yield insights into plant breeding system evolution. We studied a recently established nursery pollination interaction between native Hadena ectypa moths and introduced gynodioecious Silene vulgaris plants in North America to assess whether oviposition was biased toward females or hermaphrodites, which traits were associated with oviposition, and the effect of oviposition on host plant fitness. Oviposition was hermaphrodite‐biased and associated with deeper flowers and more stems. Sexual dimorphism in flower depth, a trait also associated with oviposition on the native host plant (Silene stellata), explained the hermaphrodite bias. Egg‐receiving plants experienced more fruit predation than plants that received no eggs, but relatively few fruits were lost, and egg receipt did not significantly alter total fruit production at the plant level. Oviposition did not enhance pollination; egg‐receiving flowers usually failed to expand and produce seeds. Together, our results suggest that H. ectypa oviposition does not exert a large fitness cost on host plants, sex‐biased interactions can emerge from preferences developed on a hermaphroditic host species, and new nursery pollination interactions can arise as negative or neutral rather than as mutualistic for the plant.