The popularity of iNaturalist and other online biodiversity databases to which the general public and specialists alike contribute observations has skyrocketed in recent years (Dance 2022). The AI-based algorithms (computer vision) which provide the first identification of a given organism on an uploaded photograph have become very sophisticated, suggesting initial identifications often down to species level with a surprisingly high degree of accuracy. The initial identifications are then confirmed or improved by feedback from the community, which works particularly well for organismal groups to which many active community members contribute, such as the birds. Hence, providing initial observations and identifying observations of others, as well as browsing the recorded biodiversity for given locales or the range of occurrences of individual taxa has become a meaningful and satisfying experience for the interested naturalist. Furthermore, several research studies have now been published relying on observations uploaded to iNaturalist (Szentivanyi and Vincze 2022). However, using the enormous amount of natural history data available on iNaturalist in a systematic way has remained challenging, since this requires not only retrieving numerous observations from the database (in the hundreds or even thousands), but also some level of transparent quality control.

Billotte (2022) provides a protocol and R scripts for the quality assessment of downloaded observations from iNaturalist, allowing an efficient and reproducible stepwise approach to prepare a high-quality data set for further analysis. First, observations with their associated metadata are downloaded from iNaturalist, along with the corresponding entries from the Global Biodiversity Information Facility (GBIF). In addition, a taxonomic reference list is obtained (these are available online for many taxa), which is used to assess the taxonomic consistency in the dataset. Second, the geo-tagging is assessed by comparing the iNaturalist and GBIF metadata. Lastly, the image quality is assessed using pyBRISQUE. The approach is illustrated using spiders (Araneae) as an example. Spiders are a very diverse taxon and an excellent taxonomic reference list is available (World Spider Catalogue 2022). However, spiders are not well known to most non-specialists, and it is not easy to take good pictures of spiders without using professional equipment. Therefore, the ability of iNaturalist’s computer vision to provide identifications is limited to this date and the community of specialists active on iNaturalist is comparatively small. Hence, spiders are a good taxon to demonstrate how the pipeline results in a quality-controlled dataset based on crowed-sourced data. Importantly, the software employed is free to use, although inevitably, the initial learning curve to use R scripts can be steep, depending on prior expertise with R/RStudio. Furthermore, the approach is employable with databases other than iNaturalist.

In summary, Billotte's (2022) pipeline allows researchers to use the wealth of observations on iNaturalist and other databases to produce large metadata and image datasets of high-quality in a reproducible way. This should pave the way for more studies, which could include, for example, the assessment of range expansions of invasive species or the evaluation of the presence of endangered species, potentially supporting conservation efforts.

References

Billotte J (2022) A pipeline for assessing the quality of images and metadata from crowd-sourced databases. BiorXiv, 2022.04.29.490112, ver 5 peer reviewed and recommended by Peer Community In Zoology. https://doi.org/10.1101/2022.04.29.490112

Dance A (2022) Community science draws on the power of the crowd. Nature, 609, 641–643. https://doi.org/10.1038/d41586-022-02921-3

Szentivanyi T, Vincze O (2022) Tracking wildlife diseases using community science: an example through toad myiasis. European Journal of Wildlife Research, 68, 74. https://doi.org/10.1007/s10344-022-01623-5

World Spider Catalog (2022). World Spider Catalog. Version 23.5. Natural History Museum Bern, online at http://wsc.nmbe.ch. https://doi.org/10.24436/2

Ticks are notorious vectors of diseases in humans and other vertebrates. Much effort has been expended to understand tick diversity and ecology with the aim of managing their populations to alleviate the misery they bring. Further, the fundamental question of whether ticks are usually host generalists or host specialists has been debated at length and is important both for understanding the mechanisms of their diversification as well as for focusing control of ticks [1].

One elegant resolution of this question is to consider most tick species to be global generalists but local specialists [1]. This is well illustrated in a series of studies of the seabird tick, Ixodes uriae, which is comprised of host-specific races that show genetic [2], morphological [3] and host performance [4] differences associated with the seabirds they feed on. Such a pattern has clear ramifications for sympatric speciation; however, the factors that potentially act to drive these differences have remained elusive.

Dupraz et al. [5] have now made intriguing and important steps toward bridging the gap between demonstrating local patterns of tick host association and understanding the physiological mechanisms that may facilitate such divergences. They collected I. uriae ticks from the nests of two seabirds – Atlantic puffins and common guillemots – on the north side of Iceland. Four populations of ticks were sampled, with one island providing both puffin ticks and guillemot ticks, to give two tick populations from each of the two seabird host species. They then washed the ticks in solvent and analyzed the dissolved cuticular hydrocarbons (CHCs) using GC mass spectrometry, revealing 22 different hydrocarbon compounds common to most of these samples. CHCs are known to be important across arthropods for a variety of functions ranging from reducing water loss to facilitating communication and recognition between individuals with species.

Dupraz et al. [5] found three hydrocarbons that distinguished puffin ticks most consistently from guillemot ticks. A cross-validation test for host type also assigned 75% of the tick pools to the seabird host of origin. However, with these limited sample sizes, statistical analysis revealed no significant difference in CHC profiles between the host types, although a tendency was evident. Nonetheless, this study revealed a number of potentially diagnostic CHCs for tick host type, as well as some that may be more diagnostic of locations. This provides a fascinating and actionable foundation for further work using additional sites and host types, as well as an entry point into discerning the mechanisms at play in producing the diversity, complexity and adaptability that make ticks such medical menaces.

References

[1]  McCoy, K.D., Léger, E., Dietrich, M., 2013. Host specialization in ticks and transmission of tick-borne diseases: a review. Front. Cell. Infect. Microbiol. 3. https://doi.org/10.3389/fcimb.2013.00057

[2]  McCoy, K.D., Chapuis, E., Tirard, C., Boulinier, T., Michalakis, Y., Bohec, C.L., Maho, Y.L., Gauthier-Clerc, M., 2005. Recurrent evolution of host-specialized races in a globally distributed parasite. Proc. R. Soc. B Biol. Sci. 272, 2389–2395. https://doi.org/10.1098/rspb.2005.3230

[3]  Dietrich, M., Beati, L., Elguero, E., Boulinier, T., McCoy, K.D., 2013. Body size and shape evolution in host races of the tick Ixodes uriae. Biol. J. Linn. Soc. 108, 323–334. https://doi.org/10.1111/j.1095-8312.2012.02021.x

[4]  Dietrich, M., Lobato, E., Boulinier, T., McCoy, K.D., 2014. An experimental test of host specialization in a ubiquitous polar ectoparasite: a role for adaptation? J. Anim. Ecol. 83, 576–587. https://doi.org/10.1111/1365-2656.12170

[5] Dupraz, M., Leroy, C., Thórarinsson, T. L., d’Ettorre, P. and McCoy, K. D. (2022) Within and among population differences in cuticular hydrocarbons in the seabird tick Ixodes uriae. bioRxiv, 2022.01.21.477272, ver. 5 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2022.01.21.477272

Polyphenisms offer an opportunity to study the links between phenotype, development, and environment in a controlled genomic context (Simpson, Sword, & Lo, 2011). In organisms with short generation times, individuals living and developing in different seasons encounter different environmental conditions. Adaptive plasticity allows them to express different phenotypes in response to seasonal cues, such as temperature or photoperiod. Such phenotypes can be morphological variants, for instance displaying different wing patterns as seen in butterflies (Brakefield & Larsen, 1984; Nijhout, 1991; Windig, 1999), or physiological variants, characterized for instance by direct development vs winter diapause in temperate insects (Dalin & Nylin, 2012; Lindestad, Wheat, Nylin, & Gotthard, 2019; Shearer et al., 2016). 

Many aphids display cyclical parthenogenesis, a remarkable seasonal polyphenism for reproductive mode (Tagu, Sabater-Muñoz, & Simon, 2005), also sometimes coupled with wing polyphenism (Braendle, Friebe, Caillaud, & Stern, 2005), which allows them to switch between parthenogenesis during spring and summer to sexual reproduction and the production of diapausing eggs before winter. In the pea aphid Acyrthosiphon pisum, photoperiod shortening results in the production, by parthenogenetic females, of embryos developing into the parthenogenetic mothers of sexual individuals. The link between parthenogenetic reproduction and sexual reproduction, therefore, occurs over two generations, changing from a parthenogenetic form producing parthenogenetic females (virginoparae), to a parthenogenetic form producing sexual offspring (sexuparae), and finally sexual forms producing overwintering eggs (Le Trionnaire et al., 2022).  

The molecular basis for the transduction of the environmental signal into reproductive changes is still unknown, but the dopamine pathway is an interesting candidate. Form-specific expression of certain genes in the dopamine pathway occurs downstream of the perception of the seasonal cue, notably with a marked decrease in the heads of embryos reared under short-day conditions and destined to become sexuparae. Dopamine has multiple roles during development, with one mode of action in cuticle melanization and sclerotization, and a neurological role as a synaptic neurotransmitter. Both modes of action might be envisioned to contribute functionally to the perception and transduction of environmental signals. 

In this study, Le Trionnaire and colleagues aim at clarifying this role in the pea aphid (Le Trionnaire et al., 2022). Using quantitative RT-PCR, RNA-seq, and in situ hybridization of RNA probes, they surveyed the timing and spatial patterns of expression of dopamine pathway genes during the development of different stages of embryo to larvae reared under long and short-day conditions, and destined to become virginoparae or sexuparae females, respectively. The genes involved in the synaptic release of dopamine generally did not show differences in expression between photoperiodic treatments. By contrast, pale and ddc, two genes acting upstream of dopamine production, generally tended to show a downregulation in sexuparare embryo, as well as genes involved in cuticle development and interacting with the dopamine pathway. The downregulation of dopamine pathway genes observed in the heads of sexuparare juveniles is already detectable at the embryonic stage, suggesting embryos might be sensing environmental cues leading them to differentiate into sexuparae females.

The way pale and ddc expression differences could influence environmental sensitivity is still unclear. The results suggest that a cuticle phenotype specifically in the heads of larvae could be explored, perhaps in the form of a reduction in cuticle sclerotization and melanization which might allow photoperiod shortening to be perceived and act on development. Although its causality might be either way, such a link would be exciting to investigate, yet the existence of cuticle differences between the two reproductive types is still a hypothesis to be tested. The lack of differences in the expression of synaptic release genes for dopamine might seem to indicate that the plastic response to photoperiod is not mediated via neurological roles. Yet, this does not rule out the role of decreasing levels of dopamine in mediating this response in the central nervous system of embryos, even if the genes regulating synaptic release are equally expressed. 

To test for a direct role of ddc in regulating the reproductive fate of embryos, the authors have generated CrispR-Cas9 knockout mutants. Those mutants displayed egg cuticle melanization, but with lethal effects, precluding testing the effect of ddc at later stages in development. Gene manipulation becomes feasible in the pea aphid, opening up certain avenues for understanding the roles of other genes during development.

This study adds nicely to our understanding of the intricate changes in gene expression involved in polyphenism. But it also shows the complexity of deciphering the links between environmental perception and changes in physiology, which mobilise multiple interacting gene networks. In the era of manipulative genetics, this study also stresses the importance of understanding the traits and phenotypes affected by individual genes, which now seems essential to piece the puzzle together.

References

Braendle C, Friebe I, Caillaud MC, Stern DL (2005) Genetic variation for an aphid wing polyphenism is genetically linked to a naturally occurring wing polymorphism. Proceedings of the Royal Society B: Biological Sciences, 272, 657–664. https://doi.org/10.1098/rspb.2004.2995

Brakefield PM, Larsen TB (1984) The evolutionary significance of dry and wet season forms in some tropical butterflies. Biological Journal of the Linnean Society, 22, 1–12. https://doi.org/10.1111/j.1095-8312.1984.tb00795.x

Dalin P, Nylin S (2012) Host-plant quality adaptively affects the diapause threshold: evidence from leaf beetles in willow plantations. Ecological Entomology, 37, 490–499. https://doi.org/10.1111/j.1365-2311.2012.01387.x

Le Trionnaire G, Hudaverdian S, Richard G, Tanguy S, Gleonnec F, Prunier-Leterme N, Gauthier J-P, Tagu D (2022) Dopamine pathway characterization during the reproductive mode switch in the pea aphid. bioRxiv, 2020.03.10.984989, ver. 4 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2020.03.10.984989

Lindestad O, Wheat CW, Nylin S, Gotthard K (2019) Local adaptation of photoperiodic plasticity maintains life cycle variation within latitudes in a butterfly. Ecology, 100, e02550. https://doi.org/10.1002/ecy.2550

Nijhout HF (1991). The development and evolution of butterfly wing patterns. Washington, DC: Smithsonian Institution Press.

Shearer PW, West JD, Walton VM, Brown PH, Svetec N, Chiu JC (2016) Seasonal cues induce phenotypic plasticity of Drosophila suzukii to enhance winter survival. BMC Ecology, 16, 11. https://doi.org/10.1186/s12898-016-0070-3

Simpson SJ, Sword GA, Lo N (2011) Polyphenism in Insects. Current Biology, 21, R738–R749. https://doi.org/10.1016/j.cub.2011.06.006

Tagu D, Sabater-Muñoz B, Simon J-C (2005) Deciphering reproductive polyphenism in aphids. Invertebrate Reproduction & Development, 48, 71–80. https://doi.org/10.1080/07924259.2005.9652172

Windig JJ (1999) Trade-offs between melanization, development time and adult size in Inachis io and Araschnia levana (Lepidoptera: Nymphalidae)? Heredity, 82, 57–68. https://doi.org/10.1038/sj.hdy.6884510

Whiteflies are serious global pests that feed on phloem sap of many agricultural crop plants. Like other phloem feeders, whiteflies rely on a primary-symbiont to supply their poor, sugar-based diet. Over time, the genomes of primary-symbionts become degraded, and they are either been replaced or complemented by co-hosted secondary-symbionts (McCutcheon and Moran 2012). In Bemisia tabaci species complex, the primary-symbiont is Candidatus Portiera aleyrodidarium, with seven secondary-symbionts that have been described to date. The prevalence and dynamics of these secondary-symbionts have been studied in various whitefly populations and genetic groups around the world, and certain combinations are determined under specific biotic and environmental factors (Zchori-Fein et al. 2014).

To understand the potential metabolic or other interactions of various secondary-symbionts with Ca. Portiera aleyrodidarium and the hosts, Mouton et al. used metabarcoding approach and diagnostic PCR confirmation, to describe symbiont compositions in a collection of whiteflies from eight populations with four genetic groups in Burkina Faso. They found that one of the previously recorded secondary-symbiont from Asian whitefly populations, Candidatus Hemipteriphilus asiaticus, is also found in the tested African whiteflies. The newly identified Ca. Hemipteriphilus asiaticus forms a different strain than the ones described in Asia, and is found in high prevalence in six of the tested populations and in three genetic groups. They also showed that Portiera densities are not affected by the presence of Ca. Hemipteriphilus asiaticus. The authors suggest that based on its high prevalence, Ca. Hemipteriphilus asiaticus may benefit certain whitefly populations, however, there is no attempt to test this assumption or to relate it to environmental factors, or to identify the source of introduction.

Mouton et al. bring new perspectives to the study of complex hemipteran symbioses, emphasizing the need to use both unbiased approaches such as metabarcoding, together with a priori methods such as PCR, in order to receive a complete description of symbiont population structures. Their findings are awaiting future screens for this secondary-symbiont, as well as its functional genomics and experimental manipulations to clarify its role. Discoveries on whitefly-symbionts delicate interactions are required to develop alternative control strategies for this worldly devastating pest.

References

McCutcheon JP, Moran NA (2012) Extreme genome reduction in symbiotic bacteria. Nature Reviews Microbiology, 10, 13–26. https://doi.org/10.1038/nrmicro2670

Mouton L, Henri H, Romba R, Belgaidi Z, Gnankiné O, Vavre F (2022) Analyses of symbiotic bacterial communities in the plant pest Bemisia tabaci reveal high prevalence of Candidatus Hemipteriphilus asiaticus on the African continent. bioRxiv, 2021.10.06.463217, ver. 3 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2021.10.06.463217

Zchori-Fein E, Lahav T, Freilich S (2014) Variations in the identity and complexity of endosymbiont combinations in whitefly hosts. Frontiers in Microbiology, 5. https://doi.org/10.3389/fmicb.2014.00310

In pollinator insects, especially bees, foraging is almost exclusively performed by females due to the close linkage with brood care. They collect pollen as a protein- and lipid-rich food to feed developing larvae in solitary and social species. Bees take carbohydrate-rich nectar in small quantities to fuel their flight and carry the pollen load. To optimise the foraging flight, they tend to be flower constant, reducing the flower handling time and time among individual inflorescences (Goulson, 1999). Males of pollinator species might be found on flowers as well. As they do not collect any pollen for brood care, their foraging flights and visits to flowers might not be shaped by the selective forces that optimise the foraging flights of females. They might stay longer in individual flowers, take up nectar if needed, but might unintentionally carry pollen on their body surface (Wolf & Moritz, 2014).
 
Bumblebees are excellent pollinators (Goulson, 2010), and a few species are exploited commercially for their delivery of pollination services (Velthuis & van Doorn, 2006). However, a monophyletic group of socially parasitic species – cuckoo bumblebees – has evolved amongst the bumblebees, lacking a worker caste. Cuckoo bee gynes usurp nests of free-living bumblebees, kill the resident queen, and forces the host workers to rear their offspring consisting of gynes and males (Lhomme & Hines, 2019). The level of affected colonies in an area can be up to 42% (Erler & Lattorff, 2010).
 
The behaviour of the cuckoo bumblebees, especially that of the males, has been rarely studied. The present study by Fisogni et al. (2021) has targeted the flower-visiting behaviour of workers and males of free-living bumblebees and males of the cuckoo species. They used behavioural observations of flower-visiting insects on Gentiana lutea, a plant from south-eastern Europe with yellow flowers arranged in whorls. While all three groups of bees visited the same number of plants, males of both types visited more flowers within a whorl, but cuckoo males spent more time on flowers within a whorl and the whole plant than the free-living bumblebees.
 
The flower visits of bumblebee workers are optimised, aiming at collecting as much pollen as possible within a short time frame. This, in turn, has consequences for the pollination process by enhancing cross-pollination between different plants. By contrast, males and especially cuckoo bumblebee males, are not selected for an optimised foraging pattern. Instead, they spend more time on flowers, eventually resulting in higher levels of pollen transfer within a plant (geitonogamy), which might lead to reduced plant fitness. This is the first study to relate the foraging behaviour of cuckoo bumblebees to pollination and plant fitness.
 
References
 
Erler, S., & Lattorff, H. M. G. (2010). The degree of parasitism of the bumblebee (Bombus terrestris) by cuckoo bumblebees (Bombus (Psithyrus) vestalis). Insectes sociaux, 57(4), 371-377. https://doi.org/10.1007/s00040-010-0093-2
 
Fisogni, A., Bogo, G., Massol, F., Bortolotti, L., Galloni, M. (2021). Cuckoo male bumblebees perform slower and longer flower visits than free-living male and worker bumblebees. Zenodo, 10.5281/zenodo.4489066, ver. 1.2 peer-reviewed and recommended by PCI Zoology. https://doi.org/10.5281/zenodo.4489066
 
Goulson, D. (1999). Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspectives in plant ecology, evolution and systematics, 2(2), 185-209. https://doi.org/10.1078/1433-8319-00070
 
Goulson, D. (2010). Bumblebees. Behaviour, Ecology, and Conservation, 2nd edn. Oxford University Press, Oxford.
 
Lhomme, P., Hines, H. M. (2019). Ecology and evolution of cuckoo bumble bees. Annals of the Entomological Society of America, 112, 122-140. https://doi.org/10.1093/aesa/say031
 
Velthuis, H. H. W., van Doorn, A. (2006). A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie, 37, 421-451. https://doi.org/10.1051/apido:2006019
 
Wolf, S., Moritz, R. F. A. (2014). The pollination potential of free-foraging bumblebee (Bombus spp.) males (Hymenoptera. Apidae). Apidologie, 45, 440-450. https://doi.org/10.1007/s13592-013-0259-9