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About
Why and how do individuals vary in their ability to reproduce?
Biography
My fascination with sexual selection was sparked during my undergraduate studies (Macquarie University, Australia) when I learned about Jonathan Waage’s work on sperm displacement in damselflies. This set me off on an adventure that has taken me around the world. I completed my PhD at the University of Chicago (USA) and a postdoctoral fellowship at Arizona State University (USA), before moving to Norway to work on sperm evolution at the Natural History Museum of Oslo. In 2014, I became a junior group leader at the University of Oslo, where my group investigated the role of microbes in the functional evolution of avian ejaculates.
In 2019, I joined the Department of Animal Ecology at NIOO-KNAW. Research in my group focuses on understanding why and how individuals vary in their ability to reproduce, with a particular focus on understanding the consequences of variation in post-copulatory sexual traits for fitness. We work primarily with passerine birds and use a wide range of methodological and analytical approaches in both field-based studies of natural populations and experimental work in captive populations.
Research groups
CV
Employment
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2019–PresentTenure Track Researcher (NIOO-KNAW)
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2014–2019Researcher at the Centre for Ecological and Evolutionary Synthesis (CEES) and Natural History Museum, University of Oslo (Norway)
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2010–2014Postdoc at the Natural History Museum, University of Oslo (Norway)
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2008–2010Postdoc at the School of Life Sciences, Arizona State University (USA)
Education
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2005–2008PhD in the Department of Ecology and Evolution, University of Chicago (USA)
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2003–2005MSc in the Department of Ecology and Evolution, University of Chicago (USA)
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1998–2000BSc (First Class Honours) in the School of Life Sciences, Macquarie University (Australia)
Publications
Key publications
Peer-reviewed publications
Systematic approaches to assessing high temperature limits to fertility in animals
Critical thermal limits (CTLs) gauge the physiological impact of temperature on survival or critical biological function, aiding predictions of species range shifts and climatic resilience. Two recent Drosophila species studies, using similar approaches to determine temperatures that induce sterility (thermal fertility limits [TFLs]), reveal that TFLs are often lower than CTLs and that TFLs better predict both current species distributions and extinction probability. Moreover, many studies show fertility is more sensitive at less extreme temperatures than survival (thermal sensitivity of fertility [TSF]). These results present a more pessimistic outlook on the consequences of climate change. However, unlike CTLs, TFL data are limited to Drosophila, and variability in TSF methods poses challenges in predicting species responses to increasing temperature. To address these data and methodological gaps, we propose 3 standardized approaches for assessing thermal impacts on fertility. We focus on adult obligate sexual terrestrial invertebrates but also provide modifications for other animal groups and life-history stages. We first outline a “gold-standard” protocol for determining TFLs, focussing on the effects of short-term heat shocks and simulating more frequent extreme heat events predicted by climate models. As this approach may be difficult to apply to some organisms, we then provide a standardized TSF protocol. Finally, we provide a framework to quantify fertility loss in response to extreme heat events in nature, given the limitations in laboratory approaches. Applying these standardized approaches across many taxa, similar to CTLs, will allow robust tests of the impact of fertility loss on species responses to increasing temperatures.https://doi.org/10.1093/jeb/voae021A systematic map of studies testing the relationship between temperature and animal reproduction
Exposure to extreme temperatures can negatively affect animal reproduction, by disrupting the ability of individuals to produce any offspring (fertility), or the number of offspring produced by fertile individuals (fecundity). This has important ecological consequences, because reproduction is the ultimate measure of population fitness: a reduction in reproductive output lowers the population growth rate and increases the extinction risk. Despite this importance, there have been no large-scale summaries of the evidence for effect of temperature on reproduction.https://doi.org/10.1002/2688-8319.12303
We provide a systematic map of studies testing the relationship between temperature and animal reproduction. We systematically searched for published studies that statistically test for a direct link between temperature and animal reproduction, in terms of fertility, fecundity or indirect measures of reproductive potential (gamete and gonad traits).
Overall, we collated a large and rich evidence base, with 1654 papers that met our inclusion criteria, encompassing 1191 species.
The map revealed several important research gaps. Insects made up almost half of the dataset, but reptiles and amphibians were uncommon, as were non-arthropod invertebrates. Fecundity was the most common reproductive trait examined, and relatively few studies measured fertility. It was uncommon for experimental studies to test exposure of different life stages, exposure to short-term heat or cold shock, exposure to temperature fluctuations, or to independently assess male and female effects. Studies were most often published in journals focusing on entomology and pest control, ecology and evolution, aquaculture and fisheries science, and marine biology. Finally, while individuals were sampled from every continent, there was a strong sampling bias towards mid-latitudes in the Northern Hemisphere, such that the tropics and polar regions are less well sampled.
This map reveals a rich literature of studies testing the relationship between temperature and animal reproduction, but also uncovers substantial missing treatment of taxa, traits, and thermal regimes. This database will provide a valuable resource for future quantitative meta-analyses, and direct future studies aiming to fill identified gaps.The role of male body size in mating success and male–male competition in a false widow spider
In many animals, body size is correlated with reproductive success. Selection sometimes generates striking differences in body size between males and females (i.e. sexual size dimorphism, SSD). SSD is common in spiders (Araneae), and is typically explained by selection for larger, more fecund females and rapidly maturing, and consequently smaller, males. Within a species males and females also often vary in body size. In the false widow spider, Steatoda grossa, females are larger than males and males trade body size for rapid development and early maturation. Moreover, males vary considerably in body size, suggesting that under certain conditions there may be advantages to large size. Here, we tested the role of male body size on mating success under noncompetitive and competitive mating conditions (i.e. male–male competition) in S. grossa. We found that body size did not influence mating success or copulation duration under noncompetitive conditions, but that larger males were more successful at obtaining access to females under competitive mating conditions. Additionally, we found that total copulation duration was significantly lower when a rival male was present. Our results show a large male advantage under male–male competition, which we suggest may contribute to the high variation in male body size observed in S. grossa. We further suggest that the reduced copulation duration observed under competitive mating conditions may have potential ramifications for male and female reproductive success and we discuss how patterns of selection acting on male body size might limit the extent of SSD in this species.https://doi.org/10.1016/j.anbehav.2023.09.011Longitudinal covariation of testosterone and sperm quality across reproductive stages in the zebra finch
https://doi.org/10.1016/j.yhbeh.2023.105388Birds that breed opportunistically maintain partial activation of reproductive systems to rapidly exploit environmental conditions when they become suitable for breeding. Maintaining reproductive systems outside of a breeding context is costly. For males, these costs are thought to include continual exposure to testosterone. Males of seasonally breeding birds minimise these costs by downregulating testosterone production outside of a breeding context. Opportunistically breeding birds trade off the need to rapidly initiate reproduction with the costs of elevated testosterone production. One way opportunistically breeding males could minimise these costs is through fine scale changes in testosterone production across discrete reproductive stages which have a greater or lesser requirement for active sperm production. Although spermatogenesis broadly depends on testosterone production, whether changes in testosterone levels across the reproductive stages affect sperm quality and production is unknown. Here, we measured testosterone, sperm quality, and body condition in male zebra finches at discrete stages within reproductive bouts (egg laying, incubation, nestling provisioning, and fledging) and across two consecutive reproductive events in captive male zebra finches (Taeniopygia castanotis). We also examined associations between male testosterone, sperm quality/production, body condition, and nestling body condition. We found that testosterone levels varied across discrete reproductive stages with the lowest levels during incubation and the highest following chick fledging. Testosterone levels were positively associated with sperm velocity and the proportion of motile sperm but were not associated with male body condition. We found no associations between paternal body condition, testosterone levels, or sperm traits with nestling body condition (a proxy for the reproductive quality of a male and his partner). This study is the first to show that opportunistically breeding males vary testosterone synthesis and sperm traits at discrete stages within a reproductive event.
Scientists' warning on climate change and insects
Climate warming is considered to be among the most serious of anthropogenicstresses to the environment, because it not only has direct effects on biodiver-sity, but it also exacerbates the harmful effects of other human-mediated threats. The associated consequences are potentially severe, particularly interms of threats to species preservation, as well as in the preservation of anarray of ecosystem services provided by biodiversity. Among the most affectedgroups of animals are insects—central components of many ecosystems—forwhich climate change has pervasive effects from individuals to communities.In this contribution to the scientists’warning series, we summarize the effectof the gradual global surface temperature increase on insects, in terms ofphysiology, behavior, phenology, distribution, and species interactions, as wellas the effect of increased frequency and duration of extreme events such as hotand cold spells, fires, droughts, and floods on these parameters. We warn that,if no action is taken to better understand and reduce the action of climatechange on insects, we will drastically reduce our ability to build a sustainablefuture based on healthy, functional ecosystems. We discuss perspectives onrelevant ways to conserve insects in the face of climate change, and we offerseveral key recommendations on management approaches that can beadopted, on policies that should be pursued, and on the involvement of thegeneral public in the protection effort.https://doi.org/10.1002/ecm.1553Experimentally testing mate preference in an avian system with unidirectional bill color introgression
https://doi.org/10.1002/ece3.9812Mating behavior can play a key role in speciation by inhibiting or facilitating gene flow between closely related taxa. Hybrid zones facilitate a direct examination of mating behavior and the traits involved in establishing species barriers. The long-tailed finch (Poephila acuticauda) has two hybridizing subspecies that differ in bill color (red and yellow), and the yellow bill phenotype appears to have introgressed ~350 km eastward following secondary contact. To examine the role of mate choice on bill color introgression, we performed behavioral assays using natural and manipulated bill colors. We found an assortative female mating preference for males of their own subspecies when bill color was not manipulated. However, we did not find this assortative preference in trials based on artificially manipulated bill color. This could suggest that assortative preference is not fixed entirely on bill color and instead may be based on a different trait (e.g., song) or a combination of traits, or alternatively may be due to lower statistical power alongside the bill manipulations being unconvincing to the female choosers. Intriguingly, we find a bias in the inheritance of bill color in captive bred F1 hybrid females. Previous modeling suggests that assortative mate preference and this kind of partial dominance in the underlying genes may together contribute to introgression, making the genetic architecture of bill color in this system a priority for future research.
Extensive transgressive gene expression in testis but not ovary in the homoploid hybrid Italian sparrow
https://doi.org/10.1111/mec.16572Hybridization can result in novel allelic combinations which can impact the hybrid phenotype through changes in gene expression. While misexpression in F1 hybrids is well documented, how gene expression evolves in stabilized hybrid taxa remains an open question. As gene expression evolves in a stabilizing manner, break-up of co-evolved cis- and trans-regulatory elements could lead to transgressive patterns of gene expression in hybrids. Here, we address to what extent gonad gene expression has evolved in an established and stable homoploid hybrid, the Italian sparrow (Passer italiae). Through comparison of gene expression in gonads from individuals of the two parental species (i.e., house and Spanish sparrow) to that of Italian sparrows, we find evidence for strongly transgressive expression in male Italian sparrows—2530 genes (22% of testis genes tested for inheritance) exhibit expression patterns outside the range of both parent species. In contrast, Italian sparrow ovary expression was similar to that of one of the parent species, the house sparrow (Passer domesticus). Moreover, the Italian sparrow testis transcriptome is 26 times as diverged from those of the parent species as the parental transcriptomes are from each other, despite being genetically intermediate. This highlights the potential for regulation of gene expression to produce novel variation following hybridization. Genes involved in mitochondrial respiratory chain complexes and protein synthesis are enriched in the subset that is over-dominantly expressed in Italian sparrow testis, suggesting that selection on key functions has moulded the hybrid Italian sparrow transcriptome.
Sperm Numbers as a Paternity Guard in a Wild Bird
https://doi.org/10.3390/cells11020231Sperm competition is thought to impose strong selection on males to produce competitive ejaculates to outcompete rival males under competitive mating conditions. Our understanding of how different sperm traits influence fertilization success, however, remains limited, especially in wild populations. Recent literature highlights the importance of incorporating multiple ejaculate traits and pre-copulatory sexually selected traits in analyses aimed at understanding how selection acts on sperm traits. However, variation in a male’s ability to gain fertilization success may also depend upon a range of social and ecological factors that determine the opportunity for mating events both within and outside of the social pair-bond. Here, we test for an effect of sperm quantity and sperm size on male reproductive success in the red-back fairy-wren (Malurus melanocephalus) while simultaneously accounting for pre-copulatory sexual selection and potential socio-ecological correlates of male mating success. We found that sperm number (i.e., cloacal protuberance volume), but not sperm morphology, was associated with reproductive success in male red-backed fairy-wrens. Most notably, males with large numbers of sperm available for copulation achieved greater within-pair paternity success. Our results suggest that males use large sperm numbers as a defensive strategy to guard within-pair paternity success in a system where there is a high risk of sperm competition and female control of copulation. Finally, our work highlights the importance of accounting for socio-ecological factors that may influence male mating opportunities when examining the role of sperm traits in determining male reproductive success.
Sperm Sizer: a program to semi-automate the measurement of sperm length
Research on sperm is incorporated into many areas of ecology and evolution including including sexual selection, reproductive physiology and ecotoxicology, as well as comparative studies in evolution and phylogenetics. Currently, producing data on sperm morphology involves several time-consuming steps, particularly photographing sperm and measuring their length (e.g. head, midpiece, tail and total sperm length). Here, we present Sperm Sizer, a freely available Java program that semi-automates the process of measuring sperm length along the centre of the sperm (including head, midpiece, tail and total length). We compare sperm measurements made with Sperm Sizer to those made with the widely used non-automated software ImageJ, for sperm from a single bird species (the long-tailed finch Poephila acuticauda), eight species of passerine bird and eight species of lizard, and provide examples demonstrating that the program can measure at least some mammalian, fish and mollusc sperm. Sperm length measurements from Sperm Sizer are highly correlated to those made using ImageJ, demonstrating that Sperm Sizer produces high quality sperm length data while taking drastically less time. Our data suggests that Sperm Sizer measurements could possibly be incorporated into existing large datasets with a small correction, although this will need to be assessed on a case-by-case basis. We suggest that generally, sperm image quality (high contrast, minimal overlap of sperm, etc.) will be more important than the shape of the sperm for whether or not Sperm Sizer is for whether or not Sperm Sizer can be employed for a given project.https://doi.org/10.1007/s00265-021-03013-4Highly variable sperm morphology in the masked finch (Poephila personata) and other estrildid finches
https://doi.org/10.1093/biolinnean/blab048Spermatozoa exhibit remarkable levels of morphological diversification among and within species. Among the passerine birds, the zebra finch (Taeniopygia guttata) has become a model system for studies of sperm biology, yet studies of closely related Estrildidae finches remain scarce. Here, we examine sperm morphology in the masked finch (Poephila personata) and place the data into the broader context of passerine sperm morphology using data for an additional 189 species. The masked finch exhibited high levels of within- and among-male variation in total sperm length and in specific sperm components. Furthermore, among-male variance in sperm length was significantly greater in estrildid (N = 12) compared with non-estrildid species (N = 178). We suggest that the high variation in sperm morphology in the masked finch and other estrildid species is likely to be linked to low levels of sperm competition, hence relaxed or weak selection on sperm length, in the clade. Our findings highlight that the highly variable sperm of the masked finch and widely studied zebra finch are 'typical' for estrildid species and stress the relevance of studying groups of closely related species. Finally, we suggest that further studies of Estrildidae will enhance our understanding of sperm diversity and avian diversity more generally.
Variation in female reproductive tract morphology across the reproductive cycle in the zebra finch
Backgroundhttps://doi.org/10.7717/peerj.10195
In seasonally breeding birds, the reproductive tract undergoes a dramatic circannual cycle of recrudescence and regression, with oviduct size increasing 5–220 fold from the non-breeding to the breeding state. Opportunistically breeding birds can produce multiple clutches sequentially across an extended period in response primarily to environmental rather than seasonal cues. In the zebra finch, it has been shown that there is a significant reduction in gonadal morphology in non-breeding females. However, the scale of recrudescence and regression of reproductive tissue within a single breeding cycle is unknown and yet important to understand the cost of breeding, and the physiological readiness to breed in such flexible breeders.
Methods
We examined the reproductive tissue of breeding female zebra finches at six stages in the nesting cycle from pre-breeding to fledging offspring. We quantified the wet mass of the oviduct, the volume of the largest pre-ovulatory follicle, and the total number of pre-ovulatory follicles present on the ovary.
Results
Measures of the female reproductive tract were highest during nesting and laying stages and declined significantly in the later stages of the breeding cycle. Importantly, we found that the mass of reproductive tissue changes as much across a single reproductive event as that previously characterized between birds categorized as breeding and non-breeding. However, the regression of the ovary is less dramatic than that seen in seasonal breeders. This could reflect low-level maintenance of reproductive tissues in opportunistic breeders, but needs to be confirmed in wild non-breeding birds.Innate and adaptive immune proteins in the preen gland secretions of male house sparrows
Recent studies have demonstrated that preen oil acts to reduce or eliminate feather‐associated bacteria. The mechanisms underlying this antibacterial activity, however, are incompletely understood. In addition to the activity of alcohols (i.e. 3,7‐dimethyloctan‐1‐ol), recent research has suggested that antimicrobial peptides may underlie the antibacterial activity of preen oil. Here, we document the presence of innate and adaptive immune proteins, lysozyme and immunoglobulin Y (IgY), in the preen oil of house sparrows Passer domesticus. We suggest lysozyme functions as an antimicrobial agent, with potentially important impacts against Gram‐positive feather degrading bacteria. Furthermore, both lysozyme and IgY likely act in local immune defence of the preen gland, and may also play a role in regulating the local microbiome, with potentially important consequences for chemical communication and signalling. Our findings suggest that the preen gland and its secretions should be considered an integral part of the body's first line of defence against invading infections.https://doi.org/10.1111/jav.02556Reproductive coordination breeds success: the importance of the partnership in avian sperm biology
Previous experience with a partner can improve reproductive coordination between a pair and increase offspring production. We paired inexperienced zebra finches and investigated how a pairs’ experience and their reproductive success together (i.e., whether they were successful or unsuccessful at rearing chicks) related to the number of sperm reaching the ovum, sperm motile performance, and hatching success. In contrast to unsuccessful pairs, successful pairs increased their relative hatching rates over sequential breeding attempts, with pairs hatching 100% of eggs after successfully fledging their previous clutch. Across the study, hatching failure was primarily due to early embryo death. Further, the number of sperm reaching the perivitelline layer (PVL) significantly decreased after fledging chicks in successful pairs, and overall, less sperm was found on the PVL in successful pairs compared with unsuccessful pairs. Across breeding attempts, males in successful pairs also exhibited a significant decline in sperm swimming speed, whereas it increased over breeding attempts in unsuccessful pairs. Our results support the idea of an optimal level of supernumerary sperm on the avian egg. However, our data suggest that there are likely to be interactions between the quality of a partnership and male sperm traits that may contribute to fitness in socially monogamous birds and that have been largely neglected to date.https://doi.org/10.1007/s00265-019-2782-9Sperm length variation among Afrotropical songbirds reflects phylogeny rather than adaptations to the tropical environment
Sperm cells vary tremendously in size and shape across the animal kingdom. In songbirds (Aves: Passeri), sperm have a characteristic helical form but vary considerably in size. Most of our knowledge about sperm morphology in this group stems from studies of species in the Northern temperate zone, while little is known about the numerous species in the tropics. Here we examined sperm size in 125 Afrotropical songbird species with emphasis on the length of the major structural components (head, midpiece, flagellum), and total sperm length measured using light microscopy. Mean total sperm length varied from 51 μm to 212 μm across species. Those belonging to the Corvoidea superfamily had relatively short sperm with a small midpiece, while those of the three major Passeridan superfamilies Passeroidea, Muscicapoidea and Sylvioidea showed large interspecific variation in total sperm length and associated variation in midpiece length. These patterns are consistent with previous findings for temperate species in the same major clades. A comparative analysis with songbird species from the Northern temperate zone (N = 139) showed large overlap in sperm length ranges although certain temperate families (e.g. Parulidae, Emberizidae) typically have long sperm and certain Afrotropical families (e.g. Cisticolidae, Estrildidae) have relatively short sperm. Afrotropical and temperate species belonging to the same families showed no consistent contrasts in sperm length. Sperm length variation among Afrotropical and Northern temperate songbirds exhibits a strong phylogenetic signal with little or no evidence for any directional latitudinal effect among closely related taxa.https://doi.org/10.1016/j.zool.2020.125770Molecular Diversification of the Seminal Fluid Proteome in a Recently Diverged Passerine Species Pair
Seminal fluid proteins (SFPs) mediate an array of postmating reproductive processes that influence fertilization and fertility. As such, it is widely held that SFPs may contribute to postmating, prezygotic reproductive barriers between closely related taxa. We investigated seminal fluid (SF) diversification in a recently diverged passerine species pair (Passer domesticus and Passer hispaniolensis) using a combination of proteomic and comparative evolutionary genomic approaches. First, we characterized and compared the SF proteome of the two species, revealing consistencies with known aspects of SFP biology and function in other taxa, including the presence and diversification of proteins involved in immunity and sperm maturation. Second, using whole-genome resequencing data, we assessed patterns of genomic differentiation between house and Spanish sparrows. These analyses detected divergent selection on immunity-related SF genes and positive selective sweeps in regions containing a number of SF genes that also exhibited protein abundance diversification between species. Finally, we analyzed the molecular evolution of SFPs across 11 passerine species and found a significantly higher rate of positive selection in SFPs compared with the rest of the genome, as well as significant enrichments for functional pathways related to immunity in the set of positively selected SF genes. Our results suggest that selection on immunity pathways is an important determinant of passerine SF composition and evolution. Assessing the role of immunity genes in speciation in other recently diverged taxa should be prioritized given the potential role for immunity-related proteins in reproductive incompatibilities in Passer sparrows.https://doi.org/10.1093/molbev/msz235
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Thesis defence Yuting Dong: effects on reproduction in a false widow spider
On 22 October 2024 NIOO researcher Yuting Dong will defend her PhD thesis "The effect of biotic and abiotic factors on reproduction in a false widow spider".
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PhD thesis defence Yuting Dong: reproduction in a false widow spider
On 22 October 2024, Yuting Dong will defend her PhD thesis, titled "The effect of biotic and abiotic factors on reproduction in a false widow spider".
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Adaptation of species
During recent centuries, human activities have dramatically changed the habitats of wild animals, plants and micro-organisms. Ecologists at NIOO are interested in how species can adapt to these rapid changes, for example through (micro)evolution. The ability of organisms to do this has a major impact on biodiversity and the functioning of ecosystems.
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‘Insects need our help in a warming world, now’
‘If no action is taken to better understand and reduce the impact of climate change on insects, we will drastically limit our chances of a sustainable future with healthy ecosystems.’ This warning in a very topical paper in Ecological Monographs comes from 70 scientists from 19 countries around the world. But, they also provide ways to help insects in a warming world complete with management strategies.
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Sperm lab
The sperm lab houses state-of-the-art equipment used for the analysis of sperm.This includes a computer-assisted sperm-analysis (CASA) system for accurate and automatic assessment of sperm motility and a microscope/camera/software combination for digital image analysis of sperm morphology.
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NIOO Theme Climate change
We are in the midst of a climate crisis. Our climate system is undergoing a dramatic number of changes, many of which can be attributed to anthropogenic influences, including greenhouse gas emission-induced changes to global surface temperatures, precipitation, glacier mass loss, sea levels, salt intrusion, and ocean heat content.
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Climate change
Our climate system is undergoing dramatic changes. We use our expertise to understand the impact on biodiversity, and the capacity of natural systems to help mitigate climate change.
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It takes more than two to tango: Microbial communities influence sex and reproduction in animals
The reproductive tracts of males and females contain whole communities of micro-organisms. These microbes can have considerable impact on (animal) fertility and reproduction, as shown by Melissah Rowe from the NIOO-KNAW.