Evolutionary Consequences of Desiccation Resistance in the Male Ejaculate

Avoiding water loss for insects is critical for survival. Selection for reduced water loss will depend on trade-offs between resources allocated for reproduction and those allocated for resisting desiccation. However, we lack knowledge on how selection for desiccation resistance can affect the male ejaculate. Furthermore, as male ejaculate composition is complex, desiccation resistant females could evolve traits that enable them to derive longevity benefits from mating. Here, we assessed how selection for desiccation resistance impacts male testes and accessory gland size, protein content of these organs, female sperm storage and male ability to inhibit female remating behavior, in the Mexican fruit fly Anastrepha ludens. Additionally, we tested if mating increased longevity and fecundity in desiccation resistant females. Males selected for resistance to desiccation stress had smaller accessory glands and seminal vesicles and females mating with these males stored less sperm compared to control males. Females mating with resistant males had lower fecundity compared to females mating with control males. Desiccation resistant females lived longer than control females, yet this was irrespective of mating. Rapid evolutionary responses to hydric stress can have correlated effects in reproductive capabilities, which are not restricted to pre-copulatory traits. Trade-offs between resistance to desiccation stress are reflected in decreased allocation of resources to reproductive organs. Thus, production of the ejaculate may be costly for A. ludens males. Knowledge on the evolution of ejaculate traits and reproductive organ size in response to directional selection for desiccation resistance, will aid our understanding of differential sex-specific responses to environmental stress.     

Mating-induced reduction in accessory reproductive organ size in the stalk-eyed fly <Emphasis Type="Italic">Cyrtodiopsis dalmanni</Emphasis>

Background  

Internal reproductive organ size is an important determinant of male reproductive success. While the response of testis length to variation in the intensity of sperm competition is well documented across many taxa, few studies address the importance of testis size in determining other components of male reproductive success (such as mating frequency) or the significance of size variation in accessory reproductive organs. Accessory gland length, but not testis length, is both phenotypically and genetically correlated with male mating frequency in the stalk-eyed fly Cyrtodiopsis dalmanni. Here we directly manipulate male mating status to investigate the effect of copulation on the size of both the testes and the accessory glands of C. dalmanni.     

Variation in male body size and reproductive allocation in the leafcutter ant <Emphasis Type="Italic">Atta colombica</Emphasis>: estimating variance components and possible trade-offs

Remarkably little is known about the traits that determine reproductive success of males in eusocial insects. Their window for mate choice decisions is very short, the actual mating process is very difficult to observe, and their small body sizes have likely prevented systematic studies in many species. In 2008 and 2009, we revisited a Panamanian population of Atta colombica leafcutter ants to partially repeat and complement a study of more than 15 years ago. We compared within- and between-colony variation in male body size (mass and width of head, mesosoma and gaster) and sperm characteristics (length, number and survival after exposure to saline buffer with and without added accessory gland secretion). We also measured the size of accessory glands as the main contributor of seminal fluid and the accessory testes containing all mature sperm, but we found few correlations between these variables. We also obtained little or no evidence for expected trade-offs between sperm number and sperm length and between mesosoma mass and sperm complement, although this could be due to limited sample size and unknown variation in larval resource allocation that was beyond our control. However, we found an interestingly bimodal distribution in broad-sense heritabilities (intra-class correlations) among the variables that we measured. Low heritabilities suggest that mesosoma size (mass and width), accessory testes size, sperm viability (measured as % survival in saline) and probably also accessory gland size are traits directly correlated with reproductive success. However, the much higher heritabilities for total body mass, gaster mass, head width, sperm length and sperm number suggest that these traits are less likely to make direct contributions to male fitness.     

Sexual selection affects the sizes of the mammalian prostate gland and seminal vesicles

The accessory reproductive glands of male mammals contribute the bulk of the secretions in which spermatozoa are transported to the female tract during copulation. Despite their morphological diversity,and the chemical complexity of their products,little is known about the possible effects of sexual selection upon these glands in mammals. Here we consider the seminal vesicles and prostate glands in a sample of 89 species and 60 genera representing 8 Orders of mammals. The sizes of the accessory glands are analysed in relation to body weight and testes weight. Both the seminal vesicles size and prostate size (corrected for body weight) correlate positively with relative testes size in this sample; this finding remains highly significant after application of procedures to correct for possible phylogenetic biases in the data set. The accessory reproductive glands are also significantly larger in those mammals which have large relative testes sizes,and in which the likelihood of sperm competition is greatest. These results support the hypothesis that sexual selection has played an important role in the evolution of the mammalian prostate gland and seminal vesicles.     

Genetic analysis of male reproductive success in relation to density in the zebrafish, Danio rerio

Background

We used behavioural and genetic data to investigate the effects of density on male reproductive success in the zebrafish, Danio rerio. Based on previous measurements of aggression and courtship behaviour by territorial males, we predicted that they would sire more offspring than non-territorial males.

Results

Microsatellite analysis of paternity showed that at low densities territorial males had higher reproductive success than non-territorial males. However, at high density territorial males were no more successful than non-territorials and the sex difference in the opportunity for sexual selection, based on the parameter I _mates, was low.

Conclusion

Male zebrafish exhibit two distinct mating tactics; territoriality and active pursuit of females. Male reproductive success is density dependent and the opportunity for sexual selection appears to be weak in this species.     

Improving breeding efficiency in potato using molecular and quantitative genetics

Key message

Potatoes are highly heterozygous and the conventional breeding of superior germplasm is challenging, but use of a combination of MAS and EBVs can accelerate genetic gain.

Abstract

Cultivated potatoes are highly heterozygous due to their outbreeding nature, and suffer acute inbreeding depression. Modern potato cultivars also exhibit tetrasomic inheritance. Due to this genetic heterogeneity, the large number of target traits and the specific requirements of commercial cultivars, potato breeding is challenging. A conventional breeding strategy applies phenotypic recurrent selection over a number of generations, a process which can take over 10 years. Recently, major advances in genetics and molecular biology have provided breeders with molecular tools to accelerate gains for some traits. Marker-assisted selection (MAS) can be effectively used for the identification of major genes and quantitative trait loci that exhibit large effects. There are also a number of complex traits of interest, such as yield, that are influenced by a large number of genes of individual small effect where MAS will be difficult to deploy. Progeny testing and the use of pedigree in the analysis can provide effective identification of the superior genetic factors that underpin these complex traits. Recently, it has been shown that estimated breeding values (EBVs) can be developed for complex potato traits. Using a combination of MAS and EBVs for simple and complex traits can lead to a significant reduction in the length of the breeding cycle for the identification of superior germplasm.     

Mitigation of inbreeding while preserving genetic gain in genomic breeding programs for outbred plants

Key message

Heuristic genomic inbreeding controls reduce inbreeding in genomic breeding schemes without reducing genetic gain.

Abstract

Genomic selection is increasingly being implemented in plant breeding programs to accelerate genetic gain of economically important traits. However, it may cause significant loss of genetic diversity when compared with traditional schemes using phenotypic selection. We propose heuristic strategies to control the rate of inbreeding in outbred plants, which can be categorised into three types: controls during mate allocation, during selection, and simultaneous selection and mate allocation. The proposed mate allocation measure GminF allocates two or more parents for mating in mating groups that minimise coancestry using a genomic relationship matrix. Two types of relationship-adjusted genomic breeding values for parent selection candidates (\({{\widetilde{\text{GEBV}}}_{\text{P}}}\)) and potential offspring (\({{\widetilde{\text{GEBV}}}_{\text{O}}}\)) are devised to control inbreeding during selection and even enabling simultaneous selection and mate allocation. These strategies were tested in a case study using a simulated perennial ryegrass breeding scheme. As compared to the genomic selection scheme without controls, all proposed strategies could significantly decrease inbreeding while achieving comparable genetic gain. In particular, the scenario using \({{\widetilde{\text{GEBV}}}_{\text{O}}}\) in simultaneous selection and mate allocation reduced inbreeding to one-third of the original genomic selection scheme. The proposed strategies are readily applicable in any outbred plant breeding program.

     

The existence of species rests on a metastable equilibrium between inbreeding and outbreeding. An essay on the close relationship between speciation, inbreeding and recessive mutations

Background

Speciation corresponds to the progressive establishment of reproductive barriers between groups of individuals derived from an ancestral stock. Since Darwin did not believe that reproductive barriers could be selected for, he proposed that most events of speciation would occur through a process of separation and divergence, and this point of view is still shared by most evolutionary biologists today.

Results

I do, however, contend that, if so much speciation occurs, the most likely explanation is that there must be conditions where reproductive barriers can be directly selected for. In other words, situations where it is advantageous for individuals to reproduce preferentially within a small group and reduce their breeding with the rest of the ancestral population. This leads me to propose a model whereby new species arise not by populations splitting into separate branches, but by small inbreeding groups "budding" from an ancestral stock. This would be driven by several advantages of inbreeding, and mainly by advantageous recessive phenotypes, which could only be retained in the context of inbreeding. Reproductive barriers would thus not arise as secondary consequences of divergent evolution in populations isolated from one another, but under the direct selective pressure of ancestral stocks. Many documented cases of speciation in natural populations appear to fit the model proposed, with more speciation occurring in populations with high inbreeding coefficients, and many recessive characters identified as central to the phenomenon of speciation, with these recessive mutations expected to be surrounded by patterns of limited genomic diversity.

Conclusions

Whilst adaptive evolution would correspond to gains of function that would, most of the time, be dominant, this type of speciation by budding would thus be driven by mutations resulting in the advantageous loss of certain functions since recessive mutations very often correspond to the inactivation of a gene. A very important further advantage of inbreeding is that it reduces the accumulation of recessive mutations in genomes. A consequence of the model proposed is that the existence of species would correspond to a metastable equilibrium between inbreeding and outbreeding, with excessive inbreeding promoting speciation, and excessive outbreeding resulting in irreversible accumulation of recessive mutations that could ultimately only lead to extinction.

Reviewer names

Eugene V. Koonin, Patrick Nosil (nominated by Dr Jerzy Jurka), Pierre Pontarotti     

Sperm competition and the evolution of male reproductive anatomy in rodents

Sperm competition is a pervasive selective force in evolution, shaping reproductive anatomy, physiology and behaviour. Here, we present comparative evidence that varying sperm competition levels account for variation in the male reproductive anatomy of rodents, the largest and most diverse mammalian order. We focus on the sperm-producing testes and the accessory reproductive glands, which produce the seminal fluid fraction of the ejaculate. We demonstrate a positive association between relative testis size and the prevalence of within-litter multiple paternity, consistent with previous analyses in which relative testis size has been found to correlate with sperm competition levels inferred from social organization and mating systems. We further demonstrate an association between sperm competition level and the relative size of at least two accessory reproductive glands: the seminal vesicles and anterior prostate. The size of the major product of these glands-the copulatory plug-is also found to vary with sperm competition level. Our findings thus suggest that selection for larger plugs under sperm competition may explain variation in accessory gland size, and highlight the need to consider both sperm and non-sperm components of the male ejaculate in the context of post-copulatory sexual selection.     

Long- term effects of previous experience determine nutrient discrimination abilities in birds

Background

The evolution of reproductive traits, such as hybrid incompatibility (postzygotic isolation) and species recognition (prezygotic isolation), have shown their key role in speciation. Theoretical modeling has recently predicted that close linkage between genes controlling pre- and postzygotic reproductive isolation could accelerate the conditions for speciation. Postzygotic isolation could develop during the sympatric speciation process contributing to the divergence of populations. Using hybrid fitness as a measure of postzygotic reproductive isolation, we empirically studied population divergence in perch (Perca fluviatilis L.) from two genetically divergent populations within a lake.

Results

During spawning time of perch we artificially created parental offspring and F₁ hybrids of the two populations and studied fertilization rate and hatching success under laboratory conditions. The combined fitness measure (product of fertilization rate and hatching success) of F₁ hybrids was significantly reduced compared to offspring from within population crosses.

Conclusion

Our results suggest intrinsic genetic incompatibility between the two populations and indicate that population divergence between two populations of perch inhabiting the same lake may indeed be promoted by postzygotic isolation.     

Is plant genetic control of ectomycorrhizal fungal communities an untapped source of stable soil carbon in managed forests?

Background

Ectomycorrhizal (ECM) fungi provide one of the main pathways for carbon (C) to move from trees into soils, where these fungi make significant contributions to microbial biomass and soil respiration.

Scope

ECM fungal species vary significantly in traits that likely influence C sequestration, such that forest C sequestration potential may be driven in part by the existing community composition of ECM fungi. Moreover, accumulating experimental data show that tree genotypes differ in their compatibility with particular ECM fungal species, i.e. mycorrhizal traits of forest trees are heritable. Those traits are genetically correlated with other traits for which tree breeders commonly select, suggesting that selection for traits of interest, such as disease resistance or growth rate, could lead to indirect selection for or against particular mycorrhizal traits of trees in forest plantations.

Conclusions

Altogether, these observations suggest that selection of particular tree genotypes could alter the community composition of symbiotic ECM fungi in managed forests, with cascading effects on soil functioning and soil C sequestration.     

Workers dominate male production in the neotropical bumblebee Bombus wilmattae (Hymenoptera: Apidae)

Background

Cooperation and conflict in social insects are closely linked to the genetic structure of the colony. Kin selection theory predicts conflict over the production of males between the workers and the queen and between the workers themselves, depending on intra-colonial relatedness but also on other factors like colony efficiency, sex ratios, cost of worker reproduction and worker dominance behaviour. In most bumblebee (Bombus) species the queen wins this conflict and often dominates male production. However, most studies in bumblebees have been conducted with only a few selected, mostly single mated species from temperate climate regions. Here we study the genetic colony composition of the facultative polyandrous neotropical bumblebee Bombus wilmattae, to assess the outcome of the queen-worker conflict over male production and to detect potential worker policing.

Results

A total of 120 males from five colonies were genotyped with up to nine microsatellite markers to infer their parentage. Four of the five colonies were queen right at point of time of male sampling, while one had an uncertain queen status. The workers clearly dominated production of males with an average of 84.9% +/- 14.3% of males being worker sons. In the two doubly mated colonies 62.5% and 96.7% of the male offspring originated from workers and both patrilines participated in male production. Inferring the mother genotypes from the male offspring, between four to eight workers participated in the production of males.

Conclusions

In this study we show that the workers clearly win the queen-worker conflict over male production in B. wilmattae, which sets them apart from the temperate bumblebee species studied so far. Workers clearly dominated male production in the singly as well the doubly mated colonies, with up to eight workers producing male offspring in a single colony. Moreover no monopolization of reproduction by single workers occurred.     

Genetic and environmental sources of covariance among internal reproductive traits in the yellow dung fly

Substantial inter- and intraspecific variation is found in reproductive traits, but the evolutionary implications of this variation remain unclear. One hypothesis is that natural selection favours female reproductive morphology that allows females to control mating and fertilization and that diverse male reproductive traits arise as counter adaptations to subvert this control. Such co-evolution predicts the establishment of genetic correlations between male and female reproductive traits that closely interact during mating. Therefore, we measured phenotypic and genetic correlations between male and female reproductive tract characteristics in the yellow dung fly, Scathophaga stercoraria (Diptera: Scathophagidae), using a nested half-sib breeding experiment. We found significant heritabilities for the size of most reproductive tract traits investigated in both females (spermathecae and their ducts, accessory glands and their ducts) and males (testis size but not sperm length). Within the sexes, phenotypic and genetic correlations were mostly nil or positive, suggesting functional integration of or condition-dependent investment in internal reproductive traits. Negative intrasexual genetic correlations, potentially suggestive of resource allocation trade-offs, were not evident. Intersexual genetic correlations were mostly positive, reflecting expected allometries between male and female morphologies. Most interestingly, testis size correlated positively with female accessory gland size and duct length, potentially indicative of a co-evolutionary arms race. We discuss these and alternative explanations for these patterns of genetic covariance.     

Limitations of microscopy to differentiate Plasmodium species in a region co-endemic for Plasmodium falciparum, Plasmodium vivax and Plasmodium knowlesi

Background

The question whether Plasmodium falciparum infection affects the fitness of mosquito vectors remains open. A hurdle for resolving this question is the lack of appropriate control, non-infected mosquitoes that can be compared to the infected ones. It was shown recently that heating P. falciparum gametocyte-infected blood before feeding by malaria vectors inhibits the infection. Therefore, the same source of gametocyte-infected blood could be divided in two parts, one heated, serving as the control, the other unheated, allowing the comparison of infected and uninfected mosquitoes which fed on exactly the same blood otherwise. However, before using this method for characterizing the cost of infection to mosquitoes, it is necessary to establish whether feeding on previously heated blood affects the survival and fecundity of mosquito females.

Methods

Anopheles gambiae M molecular form females were exposed to heated versus non-heated, parasite-free human blood to mimic blood meal on non-infectious versus infectious gametocyte-containing blood. Life history traits of mosquito females fed on blood that was heat-treated or not were then compared.

Results

The results reveal that heat treatment of the blood did not affect the survival and fecundity of mosquito females. Consistently, blood heat treatment did not affect the quantity of blood ingested.

Conclusions

The study indicates that heat inactivation of gametocyte-infected blood will only inhibit mosquito infection and that this method is suitable for quantifying the fitness cost incurred by mosquitoes upon infection by P. falciparum.     

Unfertilized frog eggs die by apoptosis following meiotic exit

Background

GGAs (Golgi-localised, γ-ear containing, ADP ribosylation factor-binding) are a family of clathrin adaptors that sort a number of biologically important transmembrane proteins into clathrin-coated vesicles. Knockout and knockdown studies to determine GGA function are confounded by the fact that there are 3 GGA genes in mammalian cells. Thus Drosophila melanogaster is a useful model system to study tissue expression profiles and knockdown phenotypes as there is a single GGA ortholog.

Results

Here we have quantified protein expression in Drosophila and show that there is >3-fold higher expression of GGA in male flies relative to female flies. In female flies the majority of GGA expression is in the head. In male flies GGA is not only expressed at high levels in the head but there is a gender specific increased expression which is due to the abundant expression of GGA in the testes. Using a highly specific antibody we have localised endogenous GGA protein in testes squashes, and visualised it in somatic and germ line cells. We show that GGA is expressed during multiple stages of sperm development, and co-stains with a marker of the trans-Golgi Network. This is most striking at the acroblast of early spermatids. In spite of the high expression of GGA in testes, knocking down its expression by >95% using transgenic RNAi fly lines did not affect male fertility. Therefore spermatogenesis in the male flies appears to progress normally with <5% GGA, most likely because alternative adaptors may be able to substitute partially or completely for the function of GGA. We also identify 'cueball' as a novel cargo for GGA, and mutants of cueball have been shown to have a male sterility phenotype.

Conclusion

In Drosophila we have uncovered a potential role for GGA in the testes of male flies. The gender specific higher expression of GGA, its specific enrichment in testes and its localisation to developing spermatocytes and at the acroblast of spermatids supports a role for GGA function in Drosophila spermatogenesis, even though spermatogenesis still occurs when GGA expression is depleted to <5% of control.