Dipteran Species Research Articles

ALKBH8 as a potential N6 -methyladenosine (m6 A) eraser in insects.

The N6 -methyladenosine (m6 A) machinery functions through three groups of proteins in eukaryotic cells, including m6 A writers, erasers and readers. The m6 A cellular machinery has mostly been characterised in mammalian species, and the relevant literature on insects is currently scant. While homologues of m6 A writers and readers have been reported from insects, no erasers have been described so far. Here, using BLAST search, we searched for potential erasers in insects. While we found homologues of human m6 A eraser ALKBH5 in termites, beetles and true bugs, they could not be found in representative dipteran and lepidopteran species. However, a potential m6 A eraser, ALKBH8, was identified and experimentally investigated. Our results showed that ALKBH8 can reduce the m6 A levels of Aedes aegypti and Drosophila melanogaster RNAs, suggesting that AeALKBH8 could be a candidate m6 A eraser in insects.

ENTOMOFAUNA DE INTERES FORENSE ASOCIADA AL PROCESO DE DESCOMPOSICIÓN CADAVÉRICA DE Sus scrofa EN ÉPOCA DE VERANO EN UN DISTRITO DEL NORTE DEL PERÚ

Necrophagous insects, mainly Diptera and Coleoptera, are involved in the cadaveric decomposition process depending on time ofstudy and location, are important to estimate the postmortem interval. Pigs have become the most frequently used animal model in forensic science. The objective of this research was to identify the genera and/or species of necrophagous insects in the five stages of the cadaveric decomposition process, at the time of summer 2018 taking place in an urban area of Nuevo Chimbote (Ancash, Peru), using SusscrofaL. as an animal model. It was used a 12-kg pig carcass, recently euthanized and kept for 70 days, at an average temperature of 24.26°C and an average relative humidity of 66.96% inside a Schoenly-type trap to capture insects. Insects of the Diptera and Coleoptera orders were found in the different phases of decomposition: In the initial phase (two days) only dipterous insects, Sarcophagasp., Chrysomyaalbiceps, Cochliomyiamacellariaand Luciliacuprinawere identified; in the phase of active putrefaction(two days) the same species of diptera and coleoptera, Necrobiarufipesand Dermestesfrischii; in the advanced putrefaction phase (three days) the same species and also Muscadomesticadiptera; in the fermentation phase (11 days) the same species and also beetle Ammophorusperuvianus; and in the skeletonization phase (52 days) only beetles Saprinussp., Necrobiarufipesand Dermestesfrischiiwere identified. The results of this study indicate that in an open environment in an urban area of Nuevo Chimbote(Ancash, Peru), in summer season (January-March), the entomofauna was associated with the decomposition of S. scrofwhich is composed of five species of the order Diptera and four of the order Coleoptera. In addition, it was possible to observe that in the initial phase only diptera were present and in the final phase (skeletation) only coleoptera, which could be used as decomposition markers.

High larval densities and high temperatures lead to a stronger immune response in the black soldier fly

Organisms are expected to invest more in their immune function when the risk of disease infection is high. However, induction of a robust immune response is costly and may not be achievable in suboptimal environments. High conspecific density could simultaneously imply high infection risk and a suboptimal environment for many insect species. We focus on the economically important dipteran species (black soldier fly, BSF) that represents the insect order that has been ignored in previous research on density effects on immunity. The experimental part of the study was carried out to evaluate the effect of larval density (three density treatments: 1, 5 and 10 larvae/cm2) and temperature (three thermal treatments: 23, 27 and 30 °C) on the immune function of BSF larvae. The larvae that were reared at high compared to low larval densities and at higher than lower temperatures had significantly higher activity of phenoloxidase, an enzyme that plays an essential role in insect immune function. Sex did not have a significant effect on phenoloxidase activity and prepupal mass, pupal mass and adult mass were not affected by the levels of phenoloxidase activity of fifth instar larvae. In addition, we give an overview of larval density effects on insect immunity and show that density-dependent prophylaxis (stronger immune response in high larval density environments) is indeed common in the results of published case studies. However, cases with no correlation between density and immunity traits were as frequent. Moreover, in more than half of the studies, qualitatively different within-species patterns in different immunity traits were observed. We conclude that BSF larvae exhibit density-dependent prophylaxis, and larvae invest more into their immune system at high larval densities and temperatures than they do at low larval densities and temperatures.

Complete Mitochondrial Genome of Piophila casei (Diptera: Piophilidae): Genome Description and Phylogenetic Implications.

Piophila casei is a flesh-feeding Diptera insect that adversely affects foodstuffs, such as dry-cured ham and cheese, and decaying human and animal carcasses. However, the unknown mitochondrial genome of P. casei can provide information on its genetic structure and phylogenetic position, which is of great significance to the research on its prevention and control. Therefore, we sequenced, annotated, and analyzed the previously unknown complete mitochondrial genome of P. casei. The complete mt genome of P. casei is a typical circular DNA, 15,785 bp in length, with a high A + T content of 76.6%. It contains 13 protein-coding genes (PCG), 2 ribosomal RNA (rRNA) genes, 22 transfer RNA (tRNA) genes, and 1 control region. Phylogenetic analysis of 25 Diptera species was conducted using Bayesian and maximum likelihood methods, and their divergence times were inferred. The comparison of the mt genomes from two morphologically similar insects P. casei and Piophila megastigmata indicates a divergence time of 7.28 MYA between these species. The study provides a reference for understanding the forensic medicine, taxonomy, and genetics of P. casei.

Biological responses of Chironomus sancticaroli to exposure to naturally aged PP microplastics under realistic concentrations.

Microplastic (MP) is yet another form of chronic anthropogenic contribution to the environment. MPs are plastic particles (<5 mm) that have been widely found in the most diverse natural environments, but their real impacts on ecosystems are still under investigation. Here, we studied the toxicity of naturally aged secondary polypropylene (PP) MPs after constant exposure to ultraviolet radiation (26 µm) to the third instar larvae of Chironomus sancticaroli, a dipteran species. The concentrations tested were 13.5; 67.5; and 135 items g-1 of dry sediment. C. sancticaroli organisms were investigated for fragment ingestion, mortality and changes in enzymatic biomarkers after 144 h of exposure. The organisms were able to ingest MPs from the first 48 h, and the amount of items internalized was dose-dependent and time-dependent. Overall, the results show that mortality was low, being significant at the lowest and highest concentrations (13.5 and 135 items g-1). Regarding changes in biochemical markers, after 144 h MDA and CAT activities were both significantly altered (increased and reduced, respectively), while SOD and GST levels were unchanged. In the present study, naturally aged polypropylene MPs induced biochemical toxicity in C. sancticaroli larvae, with toxicity being higher according to exposure time and particle concentration.

Preference of black soldier fly larvae for feed substrate previously colonised by conspecific larvae

AbstractThe black soldier fly Hermetia illucens Linnaeus (Diptera: Stratiomyidae; BSF) is gaining interest as an alternative protein ingredient for livestock feed. Larval aggregation behaviour occurs commonly in larvae of various dipteran species. However, the cues initiating aggregation behaviour and its occurrence in subsequent larval instars are still unknown in BSF larvae. Here, we focus on understanding the attraction of larvae to cues left behind in the substrate by conspecific larvae. We developed a dual‐choice test in the dark and examined the preference behaviour of different instars with the use of video recordings. Larval choices were identified based on first substrate contact, cumulative number of substrate contacts, entry of the substrate and number of larvae present in a substrate over time. Our results demonstrate that BSF larvae discriminated between similar substrates with or without cues released by conspecifics, with a strong preference for previously colonised substrates. Our results also showed a difference in behaviour between head‐capsule classes. Substrate contacts occurred more frequently in larvae from a lower head‐capsule class and the number of larvae present in a substrate over time differed between the head‐capsule classes 0.71–0.80 mm and 0.91–1.00 mm. Demonstrating arrestment in response to chemical cues from conspecifics is the first step of understanding aggregation behaviour of BSF larvae and offers opportunities to identify the chemical cues involved.

Apocrine secretion in the salivary glands of Drosophilidae and other dipterans is evolutionarily conserved.

Apocrine secretion is a transport and secretory mechanism that remains only partially characterized, even though it is evolutionarily conserved among all metazoans, including humans. The excellent genetic model organism Drosophila melanogaster holds promise for elucidating the molecular mechanisms regulating this fundamental metazoan process. Two prerequisites for such investigations are to clearly define an experimental system to investigate apocrine secretion and to understand the evolutionarily and functional contexts in which apocrine secretion arose in that system. To this end, we recently demonstrated that, in D. melanogaster, the prepupal salivary glands utilize apocrine secretion prior to pupation to deliver innate immune and defense components to the exuvial fluid that lies between the metamorphosing pupae and its chitinous case. This finding provided a unique opportunity to appraise how this novel non-canonical and non-vesicular transport and secretory mechanism is employed in different developmental and evolutionary contexts. Here we demonstrate that this apocrine secretion, which is mechanistically and temporarily separated from the exocytotic mechanism used to produce the massive salivary glue secretion (Sgs), is shared across Drosophilidae and two unrelated dipteran species. Screening more than 30 species of Drosophila from divergent habitats across the globe revealed that apocrine secretion is a widespread and evolutionarily conserved cellular mechanism used to produce exuvial fluid. Species with longer larval and prepupal development than D. melanogaster activate apocrine secretion later, while smaller and more rapidly developing species activate it earlier. In some species, apocrine secretion occurs after the secretory material is first concentrated in cytoplasmic structures of unknown origin that we name "collectors." Strikingly, in contrast to the widespread use of apocrine secretion to provide exuvial fluid, not all species use exocytosis to produce the viscid salivary glue secretion that is seen in D. melanogaster. Thus, apocrine secretion is the conserved mechanism used to realize the major function of the salivary gland in fruitflies and related species: it produces the pupal exuvial fluid that provides an active defense against microbial invasion during pupal metamorphosis.

The first complete mitochondrial genome sequences for Ulidiidae and phylogenetic analysis of Diptera.

Tetanops sintenisi is a pest that mainly damages the root of quinoa (Chenopodium quinoa) and it is first discovered in China in 2018. Here, the complete mitochondrial genome (mitogenome) of T. sintenisi was sequenced and compared with the mitogenomes of other Diptera species. The results revealed that the mitogenome of T. sintenisi is 15,763bp in length (GenBank accession number: MT795181) and is comprised of 13 protein-coding genes (PCGs), 22 transfer RNA (tRNA) genes, 2 ribosomal RNA genes, and a non-coding A + T-rich region (959bp). The highly conserved gene arrangement of the mitogenome of T. sintenisi was identical to that of other Diptera insects. Twelve PCGs contained the typical insect start codon ATN, while cox1 had CGA as the start codon. The genes cox2, nad4, and nad1 contained an incomplete termination codon T; nad3, nad5, and cob contained the complete termination codon TAG; and the remaining seven PCGs contained the termination codon TAA. All tRNA genes were predicted to fold into the typical cloverleaf secondary structure. Phylogenetic analysis of 48 species based on the mitogenome sequence revealed that T. sintenisi clustered with the Tephritidae family, indicating that T. sintenisi and Tephritidae have a close phylogenetic relationship. The phylogenetic relationship of T. sintenisi based on the mitogenome is consistent with the traditional morphological taxonomy, according to which T. sintenisi belongs to the family Otitidae, which is closely related to the family Muscidae.

On the systematic position of Cretothereva (Diptera, Therevidae): criticism versus evidence

ABSTRACT An extinct genus and species of Diptera – Cretothereva antiqua – has recently been described from the Lower Cretaceous of Brazil (Crato Formation). The fossil has been assigned to the family Therevidae and, according to its authors, would represent the oldest known member of the family of the entire Therevoid clade, with important implications for the evolutionary history of the group. A recent paper written by several Diptera experts challenges the systematic position of Cretothereva antiqua, but without a detailed assessment of the evidences. The evidence for the systematic position of this important fossil is reassessed. We argue that criticism of scientific hypotheses must be based on formal discussion of evidence, not based only on conjecture.

Diptera species, new for the Republic of Mordovia, Russia

The nature conservation depends on the completeness of the knowledge about the biodiversity in the study area. Today, data on distribution and diversity of Diptera taxa remain fragmentary. This paper supplements data on the diversity of Diptera species in Europe, Russia, and the Republic of Mordovia. We have studied 1321 specimens of 241 species collected in 2013–2022. Among them, there are species, which are new for Russia (Neoempheria brevilineata, Desmometopa discipalpis) and for both Russia and Europe (Nepphyllomyza flavescensis, Phyllomyza auriculatusa, P. luteipalpis, P. orbita, P. piceus, P. striolatum). We have found for the first time 231 Diptera species for the fauna of the Republic of Mordovia; the families of Bolitophilidae, Keroplatidae, Scatopsidae, Platypezidae, Micropezidae, Opomyzidae, Asteiidae, and Milichiidae have been found for the first time in this region. Anthrax incomptus (Bombyliidae), being previously reported for the Republic of Mordovia, has been excluded now from the fauna of this region. Nine Diptera species have been previously indicated for the Republic of Mordovia without reliable confirmation by collected specimens. In this study, we have confirmed their presence in the Republic of Mordovia. Taking into account the results of the present paper, the Diptera fauna of the Republic of Mordovia includes currently 1187 species belonging to 71 families. Data on collecting methods have been presented for the found species. We provide a comparison of collecting methods and suggestions for an effective inventory of the regional Diptera fauna. We are of the view that the number of the used collecting methods affects positively the results of the fauna inventory.

Insects Associated with the European Mistletoe (Viscum album) in Western Ukraine: a Pilot Study

The first insect-targeted study of the European mistletoe, Viscum album L., was conducted in Ukraine. In total, 35 species of insects reared from mistletoe were identified to belong to 5 orders, 20 families and 34 genera. Twenty-seven identified species were reared from mistletoe for the first time, including 17 species of Hymenoptera, 8 species of Coleoptera and 2 species of Diptera. Our results revealed significant gaps in knowledge about insects associated with mistletoe. This is appeared in the fact that more than 77 % of the insects we reared have never been detected on mistletoe before. It is obviously that 70 % to 90 % of the insects associated with mistletoe remain unknown. We also found a highly probable tripartite link between the European mistletoe, parasitic fungus Sphaeropsis visci and the saproxylic and mycetophagous Coleoptera. The in[1]teraction of Coleoptera with S. visci is facultatively mutualistic, and beetles act as vectors to spread spores and mycelium among mistletoes. In addition, we found the mass breading of invasive species Leiopus femoratus on V. album. Hence, V. album might play a crucial role in the mass and rapid invasion of L. femoratus in Europe.

The type material of Diptera (Insecta) species described by Kálmán Kertész (1867–1922)

The Hungarian dipterologist Kálmán Kertész (1867–1922), founder of the Diptera Collection of the Hungarian Natural History Museum, described 353 dipteran species new to science, and excluding three species, the type specimens of the new taxa were deposited his mother institute. The type material of 241 species has been destroyed by fire in 1956, while that of 109 species is still available. In total, 379 type specimens (34 holotypes, 271 syntypes, 11 lectotypes, 63 paralectotypes) of 109 species are available. Original combinations of scientific names of species are listed, followed by citations of the papers including the descriptions, enumerations of the type material if still available, and the currently valid names. With five figures.

Distributions of Phytophagous Syrphidae (Diptera) Species of the Lakes Region of Turkey

This study was carried out by visiting the designated areas at least twice between the months of April and October of each year between 2014 and 2016 to determine the phytophagous Syrphidae species in Antalya (Korkuteli), Afyonkarahisar (Dazkırı, Dinar), Burdur, Isparta (all districts), and Konya (Beyşehir) located within the borders of the Lakes Region. Adult syrphid individuals were collected from trees, shrubs, and herbaceous plants using sweep-net and mouth aspirator from agricultural areas, uncultivated lands and forest areas rich in vegetation and flowering plants in 46 different sampling points. As a result of the study, a total of 48 phytophagous species belonging to the genera Cheilosia (7), Eumerus (13) and Merodon (28) were found. Merodon nigritarsis (17 %), Merodon aff. bessarabicus (8 %), Merodon spinitarsis (6,25 %), Eumerus bicornis (6,16 %), Merodon crassifemoris (6,16 %) Merodon italicus (5,5 %), Merodon avidus (5 %), Cheilosia soror (3.2 %) and Merodon alagoezicus (2,6 %) were determined as the most abundant and common species.

An updated catalogue of true flies (Insecta: Diptera) from northern Pakistan

We present the first comprehensive catalogue of true flies from the northernmost territories of Pakistan, including Azad Jammu &amp; Kashmir and Gilgit-Baltistan. In the current inventory, 64 genera and 153 species in 16 families are being documented. The total number of known species has been updated based on the availability of taxonomic literatures from Pakistan. In 2007, Insect Fauna of Azad Jammu &amp; Kashmir was updated and it lists only 16 known species in order Diptera where as there is no such documented information so far available on the dipterous fauna of Gilgit-Baltistan. However, during the last few decades, relatively a few studies have been conducted on some major group of flies, i.e., Syrphidae, Sepsidae, Calliphoridae, and Tephritidae from Azad Kashmir and Gilgit-Baltistan. Among these, Syrphidae represents 53 species which is the highest number of species recorded, followed by Sepsidae and Calliphoridae with 20 and 18 species, respectively. The present diversity does not reflect the true species account in the northern areas; the important biogeographic area that exhibits a very heterogeneous fauna, not only because of the high mountains with valleys (the Hindu Kush and Karakoram ranges of the Western Himalayas) but also the junction points of the world’s two largest zoogeographical regions (the Oriental and Palaearctic). Some common families, i.e., Stratiomyidae, Asilidae, Bombyliidae, Muscidae, Conopidae, Pipinculidae, Tachinidae, and some other families which are common in high mountainous regions of northern Pakistan still need to be explored in the future studies. The complete locality data for each valid species are presented as the baseline for future studies from northern areas of Pakistan, i.e., Azad Jammu &amp; Kashmir and Gilgit-Baltistan.

An Overview of D7 Protein Structure and Physiological Roles in Blood-Feeding Nematocera.

Each time an insect bites a vertebrate host, skin and vascular injury caused by piercing triggers a series of responses including hemostasis, inflammation and immunity. In place, this set of redundant and interconnected responses would ultimately cause blood coagulation, itching and pain leading to host awareness, resulting in feeding interruption in the best-case scenario. Nevertheless, hematophagous arthropod saliva contains a complex cocktail of molecules that are crucial to the success of blood-feeding. Among important protein families described so far in the saliva of blood sucking arthropods, is the D7, abundantly expressed in blood feeding Nematocera. D7 proteins are distantly related to insect Odorant-Binding Proteins (OBP), and despite low sequence identity, observation of structural similarity led to the suggestion that like OBPs, they should bind/sequester small hydrophobic compounds. Members belonging to this family are divided in short forms and long forms, containing one or two OBP-like domains, respectively. Here, we provide a review of D7 proteins structure and function, discussing how gene duplication and some modifications in their OBP-like domains during the course of evolution lead to gain and loss of function among different hematophagous Diptera species.

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In the present investigation, 24 adult dipteran species with forensic importance belonging to 13 genera and 8 families that were collected from different localities of Iraq. The specimens were identified by different taxonomical keys; in addition the date and localities of collecting specimens were recorded.

Patterns of flower-visiting insects depend on flowering phenological shifts along an altitudinal gradient in subalpine moorland ecosystems

Alpine and subalpine moorland ecosystems contain unique plant communities, often with many endemic and threatened species, some of which depend on insect pollination. Although alpine and subalpine moorland ecosystems are vulnerable to climatic change, few studies have investigated flower-visiting insects in such ecosystems and examined the factors regulating plant-pollinator interactions along altitudinal gradients. Here, we explored how altitudinal patterns in flower visitors change according to altitudinal shifts in flowering phenology in subalpine moorland ecosystems in northern Japan. We surveyed flower-visiting insects and flowering plants at five sites differing in altitude in early July (soon after snowmelt) and mid-August (peak growing season). In July, we found a higher visiting frequency by more variable insect orders including dipteran, hymenopteran, coleopteran, and lepidopteran species at the higher altitude sites in association with the mass flowering of Geum pentapetalum and Nephrophyllidium crista-galli. In August, such altitudinal patterns were not observed, and dipteran species dominated across the sites due to the flowering of Narthecium asiaticum and Drosera rotundifolia. Our study provides key baselines for the detection of endangered biotic interactions and extinction risks of moorland plants under ongoing climate change.

Current Status of Five Warm Season Diptera Species in Estimating the Post-Mortem Interval

Abstract The accurate estimation of the time of death (Post-Mortem Interval, PMI) is of great importance when reconstructing the actual events at a crime scene following the recovery of a body. The reliability of the PMI is vital to validate witness statements and suspect alibis. The PMI estimation based on insects collected from remains relies on two fundamental principles. Firstly, the development of an insect is proportionate to its surrounding environmental condition, and secondly, colonization by insects and other arthropods typically occur according to predictable sequences subjected to seasonality, environment in which the decomposition takes place, and the possible presence of xenobiotics in the food substrate (e.g., drugs). Dipteran species of the family Calliphoridae are the most common species colonizing a corpse and carcass, and a large body of research in entomology is focused on their developmental data. Such data is used forensically to estimate the PMI via three types of calculation: accumulated degree day/hour, table of growth, and isomegalen/isomorphen diagram. Much of this research has been documented during the 20th century, in different countries, using different experimental designs and analyses. This review tabulates development data obtained from 74 manuscripts published between 1933 and 2021 for five cosmopolitan blowfly species associated with the early stages of decomposition during the warmer seasons: Chrysomya megacephala, Ch. rufifacies, Ch. albiceps, Lucilia sericata, and L. cuprina. This review highlights the importance of establishing a standardized protocol to conduct future development studies and maintaining a system for retrieval of this data for future PMI calculations.

Maggot debridement therapy and complementary wound care: a case series from Nigeria.

Maggot debridement therapy (MDT) is an emerging procedure involving the application of sterile maggots of the Dipteran species (commonly Lucilia sericata) to effect debridement, disinfection and promote healing in wounds not responding to antimicrobial therapy. Data on MDT in sub-Saharan Africa (including Nigeria) are scarce. This study aimed to use medicinal grade maggots as a complementary method to debride hard-to-heal necrotic ulcers and thereby promote wound healing. In this descriptive study, we reported on the first group of patients who had MDT at Aminu Kano Teaching Hospital (AKTH), a tertiary hospital in northern Nigeria. The first instar larvae of Lucilia sericata were applied using the confinement (free-range) maggot therapy dressing method under aseptic conditions. Diabetic foot ulcer (DFU) grade III-IV constituted more than half of the wounds (53.3%), followed by necrotising fasciitis (30%), and post-traumatic wound infection (10%). Others (6.7%, included pyomyositis, surgical site infection and post traumatic wound infection). The median surface area of the wounds was 56cm2. Of the 30 patients, half (50%) had two MDT cycles with a median time of four days. Of the wounds, 22 (73%) were completely debrided using maggots alone while eight (27%) achieved complete debridement together with surgical debridement. Wound culture pre-MDT yielded bacterial growth for all the patients and Staphylococcus aureus was the predominant isolate in 17 wounds (56.7%) while Pseudomonas aeruginosa and Streptococcus pyogenes were predominant in five wounds (16.7%) each. Only four (13.3%) wound cultures yielded bacterial growth after MDT, all Staphylococcus aureus. A good prognosis was achieved post-MDT for various wounds. MDT effectively debrides and significantly disinfects wounds involving different anatomical sites, thus enhancing wound healing and recovery. MDT is recommended in such wounds.

Paternity sharing in insects with female competition for nuptial gifts.

Male parental investment is expected to be associated with high confidence of paternity. Studies of species with exclusive male parental care have provided support for this hypothesis because mating typically co-occurs with each oviposition, allowing control over paternity and the allocation of care. However, in systems where males invest by feeding mates (typically arthropods), mating (and thus the investment) is separated from egg-laying, resulting in less control over insemination, as male ejaculates compete with rival sperm stored by females, and a greater risk of investing in unrelated offspring (cuckoldry). As strong selection on males to increase paternity would compromise the fitness of all a female's other mates that make costly nutrient contributions, paternity sharing (males not excluded from siring offspring) is an expected outcome of sperm competition. Using wild-caught females in an orthopteran and a dipteran species, in which sexually selected, ornamented females compete for male nuptial food gifts needed for successful reproduction, we examined paternity patterns and compared them with findings in other insects. We used microsatellite analysis of offspring (lifetime reproduction in the orthopteran) and stored sperm from wild-caught females in both study species. As predicted, there was evidence of shared paternity as few males failed to sire offspring. Further support for paternity sharing is the lack of last-male sperm precedence in our study species. Although paternity was not equal among sires, our estimates of paternity bias were similar to other insects with valuable nuptial gifts and contrasted with the finding that males are frequently excluded from siring offspring in species where males supply little more than sperm. This suggests paternity bias may be reduced in nuptial-gift systems and may help facilitate the evolution of these paternal investments.