Historically neglected or considered a rare aberration in animals under the biological species concept, interspecific hybridisation has by now been recognised to be taxonomically widespread, particularly in rapidly diversifying groups (Dagilis et al. 2021; Edelman & Mallet 2021; Mallet et al. 2016; Seehausen 2004). Yet the prevalence of introgressive hybridizations, its evolutionary significance, and its impact on species diversification remain a hot topic of research in evolutionary biology. The rapid increase in genomic resources now available for non-model species has significantly contributed to the detection of introgressive hybridization across taxa showing that reticulated evolution is far more common in the animal kingdom than historically considered. Yet, detecting it, quantifying its magnitude, and assessing its evolutionary significance remains a challenging endeavour with constantly evolving methodologies to better explore and exploit genomic data (Blair & Ané 2020; Degnan & Rosenberg 2009; Edelman & Mallet 2021; Hibbins & Hahn 2022).

In the marine realm, the dearth of geographic barriers and the large dispersal abilities of pelagic species like cetaceans have raised the questions of how populations and species can diverge and adapt to distinct ecological conditions in face of potentially large gene-flow, the so-called marine speciation paradox (Bierne et al. 2003). Contemporaneous hybridization among cetacean species has been widely documented in nature despite large phenotypic differences (Crossman et al. 2016). The historical prevalence of reticulated evolution, its evolutionary significance, and how it might have impacted the evolutionary history and diversification of the cetaceans have however remained elusive so far. Recent phylogenomic studies suggested that introgression has been prevalent in cetacean evolutionary history with instances reported among baleen whales (mysticetes) (Árnason et al. 2018) and among toothed whales (odontocetes), especially in the rapidly diversifying dolphins family of the Delphininae (Guo et al. 2021; Moura et al. 2020).

Analysing publicly available whole-genome data from nine cetacean species across three families of Delphinoidae – dolphins, porpoises, and monondontidae – using phylogenomics and demo-genetics approaches, Westbury and colleagues (2022) take a step further in documenting that evolution among these species has been far from a simple bifurcating tree. Instead, their study describes widespread occurrences of introgression among Delphinoidae, drawing a complex picture of reticulated evolutionary history. After describing major topology discordance in phylogenetic gene trees along the genome, the authors use a panel of approaches to disentangle introgression from incomplete lineage sorting (ILS), the two most common causes of tree topology discordances (Hibbins & Hahn 2022). Applying popular tests that separate introgression from ILS, such as the Patterson’s D (a.k.a. ABBA-BABA) test (Durand et al. 2011; Green et al. 2010), QuIBL (Edelman et al. 2019), and D-FOIL (Pease & Hahn 2015), the authors report that signals of introgression are present in the genomes of most (if not all) the cetacean species included in their study. However, this picture needs to be nuanced. Most introgression signals seem to echo old introgression events that occurred primarily among ancestors. This is suggested by the differential signals of topology discordance along the genome when considering sliding windows along the genome of varying sizes (50kb, 100kb, and 1Mb), and by patterns of excess derived allele sharing along branches of the species tree, as captured by the f-branch test (Malinsky et al. 2021; Malinsky et al. 2018). The authors further investigated the dynamic of cessation of gene flow (and/or ILS) between species using the F1 hybrid PSMC (or hPSMC) approach (Cahill et al. 2016). By estimating the cross-coalescent rates (CRR) between species pairs with time in light of previously estimated species divergence times (McGowen et al. 2020), the authors report that gene flow (and/or ILS) most likely has stopped by now among most species, but it may have lasted for more than half of the time since the species split from each other. According to the author, this result may reflect the slow process by which reproductive isolation would have evolved between cetacean lineages, and that species isolation was marked by significant introgression events.

Now, while the present study provides a good overview of how complex is the reticulated evolutionary history of the Delphinoidae, getting a complete picture will require overcoming a few important limitations. The first ones are methodological and related to the phylogenomic analyses. Given the sampling design with one diploid genome per species, the authors could not phase the data into the parental haplotypes, but instead relied on a majority consensus creating mosaic haploidized genomes representing a mixture between the two parental copies. Moreover, by using large genomic windows (≥50kb) that likely span multiple independent loci, phylogenetic analyses in windows encompassed distinct phylogenetic signals, potentially leading to bias and inaccuracy in the inferences. Thawornwattana et al (2018) previously showed that this “concatenation approach”  could significantly impact phylogenetic inferences. They proposed instead to use loci small enough to minimise the risk of intra-locus recombination and to consider them in blocks of non-recombining loci along the genome in order to conduct phylogenetic analysed, ideally under the multi-species coalescent (MSC) that can account for ILS (e.g. BPP; Flouri et al. 2018; Jiao et al. 2020; Yang 2015). Such an approach applied to the diversification of the Delphinidae may reveal substantial changes compared to the currently admitted species tree.

Inaccuracy in the species tree estimation may have a major impact on the introgression analyses conducted in this study since the species tree and branching order must be supplied in the introgression analyses to properly disentangle introgression from ILS. Here, the authors rely on the tree topology that was previously estimated in McGowen et al. (2020), which they also recovered using their consensus estimation from ASTRAL-III (Zhang et al. 2018). While the methodologies accounted to a certain extent for ILS, albeit with potential bias induced by the concatenation approach, they ignore the presumably large amount of introgression among species during the diversification process. Estimating species branching order while ignoring introgression can lead to major bias in the phylogenetic inference and can lead to incorrect topologies. Even if these MSC-based methods account for ILS, inferences can become very inaccurate or even break down as gene flow increases (see for ex. Jiao et al. 2020; Müller et al. in press; Solís-Lemus et al. 2016). Dedicated approaches have been developed to model explicitly introgression together with ILS to estimate phylogenetic networks (Blair & Ané 2020; Rabier et al. 2021) or in isolation-with-migration model (Müller et al. in press; Wang et al. 2020). Future studies revisiting the reticulated evolutionary history of the Delphinoidae with such approaches may not only precise the species branching order, but also deliver a finer view of the magnitude and prevalence of introgression during the evolutionary history of these species.

A final part of Westbury et al. (2022)'s study set out to test whether historical periods of low abundance could have facilitated hybridization among Delphinoidae species. During these periods of low abundance, species may encounter only a limited number of conspecifics and may consider individuals from other species as suitable mating partners, leading to hybridisation (Crossman et al. 2016; Edwards et al. 2011; Westbury et al. 2019). The authors tested this hypothesis by considering genome-wide genetic diversity (or heterozygosity) as a proxy of historical effective population size (Ne), itself as a proxy of the evolution of census size with time. They also try to link historical Ne variation (from PSMC, Li & Durbin 2011) with their estimated time to cessation of gene flow or ILS (from the CRR of hPSMC). However, no straightforward relationship was found between the genetic diversity and the propensity of species to hybridize, nor was there any clear link between Ne variation through time and the cessation of gene flow or ILS. Such a lack of relationship may not come as a surprise, since the determinants of genome-wide genetic diversity and its variation through evolutionary time-scale are far more diverse and complex than just a direct link with hybridization, introgression, or even with the census population size. In fact, genetic diversity results from the balance between all the evolutionary processes at play in the species' evolutionary history (see the review of Ellegren & Galtier 2016). Other important factors can strongly impact genetic diversity, including demography and structure, but also linked selection (Boitard et al. 2022; Buffalo 2021; Ellegren & Galtier 2016). 

All in all, Westbury and coll. (2022) present here an interesting study providing an additional step towards resolving and understanding the complex evolutionary history of the Delphinoidae, and shedding light on the importance of introgression during the diversification of these cetacean species. Prospective work improving upon the taxonomic sampling, with additional genomic data for each species, considered with dedicated approaches tailored at estimating species tree or network while accounting for ILS and introgression will be key for refining the picture depicted in this study. Down the road, altogether these studies will contribute to assessing the evolutionary significance of introgression on the diversification of Delphinoides, and more generally on the diversification of cetacean species, which still remain an open and exciting perspective. 

References

Árnason Ú, Lammers F, Kumar V, Nilsson MA, Janke A (2018) Whole-genome sequencing of the blue whale and other rorquals finds signatures for introgressive gene flow. Science Advances 4, eaap9873. https://doi.org/10.1126/sciadv.aap9873

Bierne N, Bonhomme F, David P (2003) Habitat preference and the marine-speciation paradox. Proceedings of the Royal Society of London. Series B: Biological Sciences 270, 1399-1406. https://doi.org/10.1098/rspb.2003.2404

Blair C, Ané C (2020) Phylogenetic Trees and Networks Can Serve as Powerful and Complementary Approaches for Analysis of Genomic Data. Systematic Biology 69, 593-601. https://doi.org/10.1093/sysbio/syz056

Boitard S, Arredondo A, Chikhi L, Mazet O (2022) Heterogeneity in effective size across the genome: effects on the inverse instantaneous coalescence rate (IICR) and implications for demographic inference under linked selection. Genetics 220, iyac008. https://doi.org/10.1093/genetics/iyac008

Buffalo V (2021) Quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain Lewontin's Paradox. e-Life 10, e67509. https://doi.org/10.7554/eLife.67509

Cahill JA, Soares AE, Green RE, Shapiro B (2016) Inferring species divergence times using pairwise sequential Markovian coalescent modelling and low-coverage genomic data. Philos Trans R Soc Lond B Biol Sci 371, 20150138. https://doi.org/10.1098/rstb.2015.0138

Crossman CA, Taylor EB, Barrett‐Lennard LG (2016) Hybridization in the Cetacea: widespread occurrence and associated morphological, behavioral, and ecological factors. Ecology and Evolution 6, 1293-1303. https://doi.org/10.1002/ece3.1913

Dagilis AJ, Peede D, Coughlan JM, Jofre GI, D’Agostino ERR, Mavengere H, Tate AD, Matute DR (2021) 15 years of introgression studies: quantifying gene flow across Eukaryotes. biorXiv, 2021.1106.1115.448399. https://doi.org/10.1101/2021.06.15.448399

Degnan JH, Rosenberg NA (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol 24, 332-340. https://doi.org/10.1016/j.tree.2009.01.009

Durand EY, Patterson N, Reich D, Slatkin M (2011) Testing for ancient admixture between closely related populations. Mol Biol Evol 28, 2239-2252. https://doi.org/10.1093/molbev/msr048

Edelman NB, Frandsen PB, Miyagi M, Clavijo B, Davey J, Dikow RB, Garcia-Accinelli G, Van Belleghem SM, Patterson N, Neafsey DE, Challis R, Kumar S, Moreira GRP, Salazar C, Chouteau M, Counterman BA, Papa R, Blaxter M, Reed RD, Dasmahapatra KK, Kronforst M, Joron M, Jiggins CD, McMillan WO, Di Palma F, Blumberg AJ, Wakeley J, Jaffe D, Mallet J (2019) Genomic architecture and introgression shape a butterfly radiation. Science 366, 594-599. https://doi.org/10.1126/science.aaw2090

Edelman NB, Mallet J (2021) Prevalence and Adaptive Impact of Introgression. Annual Review of Genetics 55, 265-283. https://doi.org/10.1146/annurev-genet-021821-020805

Edwards CJ, Suchard MA, Lemey P, Welch JJ, Barnes I, Fulton TL, Barnett R, O'Connell TC, Coxon P, Monaghan N, Valdiosera CE, Lorenzen ED, Willerslev E, Baryshnikov GF, Rambaut A, Thomas MG, Bradley DG, Shapiro B (2011) Ancient hybridization and an Irish origin for the modern polar bear matriline. Curr Biol 21, 1251-1258. https://doi.org/10.1016/j.cub.2011.05.058

Ellegren H, Galtier N (2016) Determinants of genetic diversity. Nat Rev Genet 17, 422-433. https://doi.org/10.1038/nrg.2016.58

Flouri T, Jiao X, Rannala B, Yang Z (2018) Species Tree Inference with BPP Using Genomic Sequences and the Multispecies Coalescent. Mol Biol Evol 35, 2585-2593. https://doi.org/10.1093/molbev/msy147

Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MH, Hansen NF, Durand EY, Malaspinas AS, Jensen JD, Marques-Bonet T, Alkan C, Prufer K, Meyer M, Burbano HA, Good JM, Schultz R, Aximu-Petri A, Butthof A, Hober B, Hoffner B, Siegemund M, Weihmann A, Nusbaum C, Lander ES, Russ C, Novod N, Affourtit J, Egholm M, Verna C, Rudan P, Brajkovic D, Kucan Z, Gusic I, Doronichev VB, Golovanova LV, Lalueza-Fox C, de la Rasilla M, Fortea J, Rosas A, Schmitz RW, Johnson PLF, Eichler EE, Falush D, Birney E, Mullikin JC, Slatkin M, Nielsen R, Kelso J, Lachmann M, Reich D, Paabo S (2010) A draft sequence of the Neandertal genome. Science 328, 710-722. https://doi.org/10.1126/science.1188021

Guo W, Sun D, Cao Y, Xiao L, Huang X, Ren W, Xu S, Yang G (2021) Extensive Interspecific Gene Flow Shaped Complex Evolutionary History and Underestimated Species Diversity in Rapidly Radiated Dolphins. Journal of Mammalian Evolution 29, 353-367. https://doi.org/10.1007/s10914-021-09581-6

Hibbins MS, Hahn MW (2022) Phylogenomic approaches to detecting and characterizing introgression. Genetics 220, iyab173. https://doi.org/10.1093/genetics/iyab173

Jiao X, Flouri T, Rannala B, Yang Z (2020) The Impact of Cross-Species Gene Flow on Species Tree Estimation. Syst Biol 69, 830-847. https://doi.org/10.1093/sysbio/syaa001

Li H, Durbin R (2011) Inference of human population history from individual whole-genome sequences. Nature 475, 493-496. https://doi.org/10.1038/nature10231

Malinsky M, Matschiner M, Svardal H (2021) Dsuite - Fast D-statistics and related admixture evidence from VCF files. Mol Ecol Resour 21, 584-595. https://doi.org/10.1111/1755-0998.13265

Malinsky M, Svardal H, Tyers AM, Miska EA, Genner MJ, Turner GF, Durbin R (2018) Whole-genome sequences of Malawi cichlids reveal multiple radiations interconnected by gene flow. Nature Ecology & Evolution 2, 1940-1955. https://doi.org/10.1038/s41559-018-0717-x

Mallet J, Besansky N, Hahn MW (2016) How reticulated are species? Bioessays 38, 140-149. https://doi.org/10.1002/bies.201500149 

McGowen MR, Tsagkogeorga G, Alvarez-Carretero S, Dos Reis M, Struebig M, Deaville R, Jepson PD, Jarman S, Polanowski A, Morin PA, Rossiter SJ (2020) Phylogenomic Resolution of the Cetacean Tree of Life Using Target Sequence Capture. Syst Biol 69, 479-501. https://doi.org/10.1093/sysbio/syz068

Moura AE, Shreves K, Pilot M, Andrews KR, Moore DM, Kishida T, Möller L, Natoli A, Gaspari S, McGowen M, Chen I, Gray H, Gore M, Culloch RM, Kiani MS, Willson MS, Bulushi A, Collins T, Baldwin R, Willson A, Minton G, Ponnampalam L, Hoelzel AR (2020) Phylogenomics of the genus Tursiops and closely related Delphininae reveals extensive reticulation among lineages and provides inference about eco-evolutionary drivers. Molecular Phylogenetics and Evolution 146,107047. https://doi.org/10.1016/j.ympev.2020.106756

Müller NF, Ogilvie HA, Zhang C, Fontaine MC, Amaya-Romero JE, Drummond AJ, Stadler T (in press) Joint inference of species histories and gene flow. Syst Biol.

Pease JB, Hahn MW (2015) Detection and Polarization of Introgression in a Five-Taxon Phylogeny. Syst Biol 64, 651-662. https://doi.org/10.1093/sysbio/syv023

Rabier CE, Berry V, Stoltz M, Santos JD, Wang W, Glaszmann JC, Pardi F, Scornavacca C (2021) On the inference of complex phylogenetic networks by Markov Chain Monte-Carlo. PLoS Comput Biol 17, e1008380. https://doi.org/10.1371/journal.pcbi.1008380

Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19, 198-207. https://doi.org/10.1016/j.tree.2004.01.003

Solís-Lemus C, Yang M, Ané C (2016) Inconsistency of Species Tree Methods under Gene Flow. Syst Biol 65, 843-851. https://doi.org/10.1093/sysbio/syw030

Thawornwattana Y, Dalquen D, Yang Z, Tamura K (2018) Coalescent Analysis of Phylogenomic Data Confidently Resolves the Species Relationships in the Anopheles gambiae Species Complex. Molecular Biology and Evolution 35, 2512-2527. https://doi.org/10.1093/molbev/msy158

Wang K, Mathieson I, O’Connell J, Schiffels S (2020) Tracking human population structure through time from whole genome sequences. PLOS Genetics 16, e1008552. https://doi.org/10.1371/journal.pgen.1008552

Westbury MV, Cabrera AA, Rey-Iglesia A, Cahsan BD, Duchêne DA, Hartmann S, Lorenzen ED (2022) A genomic assessment of the marine-speciation paradox within the toothed whale superfamily Delphinoidea. bioRxiv, 2020.10.23.352286, ver. 7 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2020.10.23.352286

Westbury MV, Petersen B, Lorenzen ED (2019) Genomic analyses reveal an absence of contemporary introgressive admixture between fin whales and blue whales, despite known hybrids. PLoS ONE 14, e0222004. https://doi.org/10.1371/journal.pone.0222004

Yang Z (2015) The BPP program for species tree estimation and species delimitation. Current Zoology 61, 854-865. https://doi.org/10.1093/czoolo/61.5.854

Zhang C, Rabiee M, Sayyari E, Mirarab S (2018) ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19, 153. https://doi.org/10.1186/s12859-018-2129-y

Occasional events of asexual reproduction in otherwise sexual taxa have been documented since a long time. Accounts range from observations of offspring development from unfertilized eggs in Drosophila to rare offspring production by isolated females in lizards and birds (e.g., Stalker 1954, Watts et al 2006, Ryder et al. 2021). Many more such cases likely await documentation, as rare events are inherently difficult to observe. These rare events of asexual reproduction are often associated with low offspring fitness (“tychoparthenogenesis”), and have mostly been discarded in the evolutionary literature as reproductive accidents without evolutionary significance. Recently, however, there has been an increased interest in the details of evolutionary transitions from sexual to asexual reproduction (e.g., Archetti 2010, Neiman et al.2014, Lenormand et al. 2016), because these details may be key to understanding why successful transitions are rare, why they occur more frequently in some groups than in others, and why certain genetic mechanisms of ploidy maintenance or ploidy restoration are more often observed than others. In this context, the hypothesis has been formulated that regular or even obligate asexual reproduction may evolve from these rare events of asexual reproduction (e.g., Schwander et al. 2010).

A new study by Capdevielle Dulac et al. (2022) now investigates this question in a parasitoid wasp, highlighting also the fact that what is considered rare or occasional may differ from one system to the next. The results show “rare” parthenogenetic production of diploid daughters occurring at variable frequencies (from zero to 2 %) in different laboratory strains, as well as in a natural population. They also demonstrate parthenogenetic production of female offspring in both virgin females and mated ones, as well as no reduced fecundity of parthenogenetically produced offspring. These findings suggest that parthenogenetic production of daughters, while still being rare, may be a more regular and less deleterious reproductive feature in this species than in other cases of occasional asexuality. Indeed, haplodiploid organisms, such as this parasitoid wasp have been hypothesized to facilitate evolutionary transitions to asexuality (Neimann et al. 2014, Van Der Kooi et al. 2017). First, in haploidiploid organisms, females are diploid and develop from normal, fertilized eggs, but males are haploid as they develop parthenogenetically from unfertilized eggs. This means that, in these species, fertilization is not necessarily needed to trigger development, thus removing one of the constraints for transitions to obligate asexuality (Engelstädter 2008, Vorburger 2014). Second, spermatogenesis in males occurs by a modified meiosis that skips the first meiotic division (e.g., Ferree et al. 2019). Haploidiploid organisms may thus have a potential route for an evolutionary transition to obligate parthenogenesis that is not available to organisms: The pathways for the modified meiosis may be re-used for oogenesis, which might result in unreduced, diploid eggs. Third, the particular species studied here regularly undergoes inbreeding by brother-sister mating within their hosts. Homozygosity, including at the sex determination locus (Engelstädter 2008), is therefore expected to have less negative effects in this species compared to many other, non-inbreeding haplodipoids (see also Little et al. 2017). This particular species may therefore be less affected by loss of heterozygosity, which occurs in a fashion similar to self-fertilization under many forms of non-clonal parthenogenesis. 

Indeed, the study also addresses the mechanisms underlying parthenogenesis in the species. Surprisingly, the authors find that parthenogenetically produced females are likely produced by two distinct genetic mechanisms. The first results in clonality (maintenance of the maternal genotype), whereas the second one results in a loss of heterozygosity towards the telomeres, likely due to crossovers occurring between the centromeres and the telomeres. Moreover, bacterial infections appear to affect the propensity of parthenogenesis but are unlikely the primary cause. Together, the finding suggests that parthenogenesis is a variable trait in the species, both in terms of frequency and mechanisms. It is not entirely clear to what degree this variation is heritable, but if it is, then these results constitute evidence for low-frequency existence of variable and heritable parthenogenesis phenotypes, that is, the raw material from which evolutionary transitions to more regular forms of parthenogenesis may occur.

 

References

Archetti M (2010) Complementation, Genetic Conflict, and the Evolution of Sex and Recombination. Journal of Heredity, 101, S21–S33. https://doi.org/10.1093/jhered/esq009

Capdevielle Dulac C, Benoist R, Paquet S, Calatayud P-A, Obonyo J, Kaiser L, Mougel F (2022) Spontaneous parthenogenesis in the parasitoid wasp Cotesia typhae: low frequency anomaly or evolving process? bioRxiv, 2021.12.13.472356, ver. 6 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.12.13.472356

Engelstädter J (2008) Constraints on the evolution of asexual reproduction. BioEssays, 30, 1138–1150. https://doi.org/10.1002/bies.20833

Ferree PM, Aldrich JC, Jing XA, Norwood CT, Van Schaick MR, Cheema MS, Ausió J, Gowen BE (2019) Spermatogenesis in haploid males of the jewel wasp Nasonia vitripennis. Scientific Reports, 9, 12194. https://doi.org/10.1038/s41598-019-48332-9

van der Kooi CJ, Matthey-Doret C, Schwander T (2017) Evolution and comparative ecology of parthenogenesis in haplodiploid arthropods. Evolution Letters, 1, 304–316. https://doi.org/10.1002/evl3.30

Lenormand T, Engelstädter J, Johnston SE, Wijnker E, Haag CR (2016) Evolutionary mysteries in meiosis. Philosophical Transactions of the Royal Society B: Biological Sciences, 371, 20160001. https://doi.org/10.1098/rstb.2016.0001

Little CJ, Chapuis M-P, Blondin L, Chapuis E, Jourdan-Pineau H (2017) Exploring the relationship between tychoparthenogenesis and inbreeding depression in the Desert Locust, Schistocerca gregaria. Ecology and Evolution, 7, 6003–6011. https://doi.org/10.1002/ece3.3103

Neiman M, Sharbel TF, Schwander T (2014) Genetic causes of transitions from sexual reproduction to asexuality in plants and animals. Journal of Evolutionary Biology, 27, 1346–1359. https://doi.org/10.1111/jeb.12357

Ryder OA, Thomas S, Judson JM, Romanov MN, Dandekar S, Papp JC, Sidak-Loftis LC, Walker K, Stalis IH, Mace M, Steiner CC, Chemnick LG (2021) Facultative Parthenogenesis in California Condors. Journal of Heredity, 112, 569–574. https://doi.org/10.1093/jhered/esab052

Schwander T, Vuilleumier S, Dubman J, Crespi BJ (2010) Positive feedback in the transition from sexual reproduction to parthenogenesis. Proceedings of the Royal Society B: Biological Sciences, 277, 1435–1442. https://doi.org/10.1098/rspb.2009.2113

Stalker HD (1954) Parthenogenesis in Drosophila. Genetics, 39, 4–34. https://doi.org/10.1093/genetics/39.1.4

Vorburger C (2014) Thelytoky and Sex Determination in the Hymenoptera: Mutual Constraints. Sexual Development, 8, 50–58. https://doi.org/10.1159/000356508

Watts PC, Buley KR, Sanderson S, Boardman W, Ciofi C, Gibson R (2006) Parthenogenesis in Komodo dragons. Nature, 444, 1021–1022. https://doi.org/10.1038/4441021a

Organisms often show robustness to genetic or environmental perturbations. Whether these two components of robustness can evolve separately is the focus of the paper by Le Rouzic [1]. Using theoretical analysis and individual-based computer simulations of a gene regulatory network model, he shows that multiple aspects of robustness can be investigated as a set of pleiotropically linked quantitative traits. While genetically correlated, various robustness components (e.g., mutational, developmental, homeostasis) of gene expression in the regulatory network evolved more or less independently from each other under directional selection. The quantitative approach of Le Rouzic could explain both how unselected robustness components can respond to selection on other components and why various robustness-related features seem to have their own evolutionary history. Moreover, he shows that all components were evolvable, but not all to the same extent. Robustness to environmental disturbances and gene expression stability showed the largest responses while increased robustness to genetic disturbances was slower. Interestingly, all components were positively correlated and remained so after selection for increased or decreased robustness.

This study is an important contribution to the discussion of the evolution of robustness in biological systems. While it has long been recognized that organisms possess the ability to buffer genetic and environmental perturbations to maintain homeostasis (e.g., canalization [2]), the genetic basis and evolutionary routes to robustness and canalization are still not well understood. Models of regulatory gene networks have often been used to address aspects of robustness evolution (e.g., [3]). Le Rouzic [1] used a gene regulatory network model derived from Wagner’s model [4]. The model has as end product the expression level of a set of genes influenced by a set of regulatory elements (e.g., transcription factors). The level and stability of expression are a property of the regulatory interactions in the network.

Le Rouzic made an important contribution to the study of such gene regulation models by using a quantitative genetics approach to the evolution of robustness. He crafted a way to assess the mutational variability and selection response of the components of robustness he was interested in. Le Rouzic’s approach opens avenues to investigate further aspects of gene network evolutionary properties, for instance to understand the evolution of phenotypic plasticity.

Le Rouzic also discusses ways to measure his different robustness components in empirical studies. As the model is about gene expression levels at a set of protein-coding genes influenced by a set of regulatory elements, it naturally points to the possibility of using RNA sequencing to measure the variation of gene expression in know gene networks and assess their robustness. Robustness could then be studied as a multidimensional quantitative trait in an experimental setting.

References

[1] Le Rouzic, A (2022) Gene network robustness as a multivariate character. arXiv: 2101.01564, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://arxiv.org/abs/2101.01564

[2] Waddington CH (1942) Canalization of Development and the Inheritance of Acquired Characters. Nature, 150, 563–565. https://doi.org/10.1038/150563a0

[3] Draghi J, Whitlock M (2015) Robustness to noise in gene expression evolves despite epistatic constraints in a model of gene networks. Evolution, 69, 2345–2358. https://doi.org/10.1111/evo.12732

[4] Wagner A (1994) Evolution of gene networks by gene duplications: a mathematical model and its implications on genome organization. Proceedings of the National Academy of Sciences, 91, 4387–4391. https://doi.org/10.1073/pnas.91.10.4387

We currently live in the Anthropocene, the geological age characterized by a profound impact of human populations in the ecosystems and the environment. While there is little doubt about the action of humans in the shaping of present landscapes, it can be difficult to determine what the state of those landscapes was before humans started to modify them. This is the case of the Madagascar grasslands, whose origins have been debated with arguments proposing them either as anthropogenic, created with the arrival of humans around 2000BP, or as ancient features of the natural landscape with a forest fragmentation process due to environmental changes pre-dating human arrival [e.g. 1,2]. One way to clarify this question is through the genetic study of native species. Population continuity and fragmentation along time shape the structure of the genetic diversity in space. Species living in a uniform continuous habitat are expected to show genetic structuring determined only by geographical distance. Recent changes of the habitat can take many generations to reshape that genetic structure [3]. Thus, we expect genetic structure to reflect ancient features of the landscape.

The work by Jordi Salmona and collaborators [4] studies the factors determining the population genetic structure of the Malagasy spiny olive (Noronhia spinifolia). This narrow endemic species is distributed in the discontinuous forest patches of the Loky-Manambato region (northern Madagascar). Jordi Salmona and collaborators genotyped 72 individuals distributed across the species distribution with restriction associated DNA sequencing and organelle microsatellite markers. Then, they studied the population genetic structure of the species. Using isolation-by-resistance models [5], they tested the influence of several landscape features (forest cover, roads, rivers, slope, etc.) on the connectivity between populations. Maternally inherited loci (chloroplast and mitochondria) and bi-parentally inherited loci (nuclear), were analysed separately in an attempt to identify the role of pollen and seed dispersal in the connectivity of populations.

Despite the small distribution of the species, Jordi Salmona and collaborators [4] found remarkable levels of genetic diversity. The spatial structure of this diversity was found to be mainly explained by the forest cover of the landscape, suggesting that the landscape has been composed by patches of forests and grasslands for a long time. The main role of forest cover for the connectivity among populations also highlights the importance of riparian forest as dispersal corridors. Finally, differences between organelle and nuclear markers were not enough to establish any strong conclusion about the differences between pollen and seed dispersal.

The results presented by Jordi Salmona and collaborators [4] contribute to the understanding of the history and ecology of understudied Madagascar ecosystems. Previous population genetic studies  in some forest-dwelling mammals have been interpreted as supporting an old age for the fragmented landscapes in northern Madagascar [e.g. 1,6]. To my knowledge, this is the first study on a tree species. While this work might not completely settle the debate, it emphasizes the importance of studying a diversity of species to understand the biogeographic dynamics of a region.

References

1. Quéméré, E., X. Amelot, J. Pierson, B. Crouau-Roy, L. Chikhi (2012) Genetic data suggest a natural prehuman origin of open habitats in northern Madagascar and question the deforestation narrative in this region. Proceedings of the National Academy of Sciences of the United States of
America 109: 13028–13033. https://doi.org/10.1073/pnas.1200153109
2. Joseph, G.S., C.L. Seymour (2020) Madagascan highlands: originally woodland and forest containing endemic grasses, not grazing-adapted grassland. Proceedings of the Royal Society B: Biological Sciences 287: 20201956. https://doi.org/10.1098/rspb.2020.1956
3. Landguth, E.L., S.A. Cushman, M.K. Schwartz, K.S. McKelvey, M. Murphy, G. Luikart (2010) Quantifying the lag time to detect barriers in landscape genetics. Molecular Ecology 19: 4179–
4191. https://doi.org/10.1111/j.1365-294X.2010.04808.x
4. Salmona J., Dresen A, Ranaivoson AE, Manzi S, Pors BL, Hong-Wa C, Razanatsoa J, Andriaholinirina NV, Rasoloharijaona S, Vavitsara M-E, Besnard G (2021) How ancient forest fragmentation and riparian connectivity generate high levels of genetic diversity in a micro-endemic Malagasy tree. bioRxiv, 2020.11.25.394544, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2020.11.25.394544
5. McRae, B.H. (2006) Isolation by resistance. Evolution 60: 1551–1561. https://doi.org/10.1111/j.0014-3820.2006.tb00500.x
6. Rakotoarisoa J.-E., M. Raheriarisena, S.M. Goodman (2013) Late Quaternary climatic vegetational shifts in an ecological transition zone of northern Madagascar: insights from genetic analyses of two endemic rodent species. Journal of Evolutionary Biology 26: 1019–1034. https://doi.org/10.1111/jeb.12116

Each individual multicellular organism, each of our bodies, is a small universe. Every living surface -skin, cuticle, bark, mucosa- is the home place to milliards of bacteria, fungi and viruses. They constitute our microbiota. Some of them are essential for certain organisms. Other could not live without their hosts. For many species, the relationship between host and microbiota is so close that their histories are inseparable. The recognition of this biological inextricability has led to the notion of holobiont as the organism ensemble of host and microbiota. When individuals of a particular animal or plant species expand their geographical range, it is the holobiont that expands. And these processes of migration, expansion and colonization are often accompanied by evolutionary and ecological innovations in the interspecies relationships, at the macroscopic level (e.g. novel predator-prey or host-parasite interactions) and at the microscopic level (e.g. changes in the microbiota composition). From the human point of view, these novel interactions can be economically disastrous if they involve and threaten important crop or cattle species. And this is especially worrying in the present context of genetic standardization and intensification for mass-production on the one hand, and of climate change on the other.

With this perspective, the international team led by Amandine Cornille presents a study aiming at understanding the evolutionary history of the rosy apple aphid Dysaphis plantaginea Passerini, a major pest of the cultivated apple tree Malus domestica Borkh (1). The apple tree was probably domesticated in Central Asia, and later disseminated by humans over the world in different waves, and it was probably introduced in Europe by the Greeks. It is however unclear when and where D. plantaginea started parasitizing the cultivated apple tree. The ancestral D. plantaginea could have already infected the wild ancestor of current cultivated apple trees, but the aphid is not common in Central Asia. Alternatively, it may have gained access only later to the plant, possibly via a host jump, from Pyrus to Malus that may have occurred in Asia Minor or in the Caucasus. In the present preprint, Olvera-Vázquez and coworkers have analysed over 650 D. plantaginea colonies from 52 orchards in 13 countries, in Western, Central and Eastern Europe as well as in Morocco and the USA. The authors have analysed the genetic diversity in the sampled aphids, and have characterized as well the composition of the associated endosymbiont bacteria. The analyses detect substantial recent admixture, but allow to identify aphid subpopulations slightly but significantly differentiated and isolated by distance, especially those in Morocco and the USA, as well as to determine the presence of significant gene flow. This process of colonization associated to gene flow is most likely indirectly driven by human interactions. Very interestingly, the data show that this genetic diversity in the aphids is not reflected by a corresponding diversity in the associated microbiota, largely dominated by a few Buchnera aphidicola variants. In order to determine polarity in the evolutionary history of the aphid-tree association, the authors have applied approximate Bayesian computing and machine learning approaches. Albeit promising, the results are not sufficiently robust to assess directionality nor to confidently assess the origin of the crop pest. Despite the large effort here communicated, the authors point to the lack of sufficient data (in terms of aphid isolates), especially originating from Central Asia. Such increased sampling will need to be implemented in the future in order to elucidate not only the origin and the demographic history of the interaction between the cultivated apple tree and the rosy apple aphid. This knowledge is needed to understand how this crop pest struggles with the different seasonal and geographical selection pressures while maintaining high genetic diversity, conspicuous gene flow, differentiated populations and low endosymbiontic diversity.

References

1. Olvera-Vazquez SG, Remoué C, Venon A, Rousselet A, Grandcolas O, Azrine M, Momont L, Galan M, Benoit L, David GM, Alhmedi A, Beliën T, Alins G, Franck P, Haddioui A, Jacobsen SK, Andreev R, Simon S, Sigsgaard L, Guibert E, Tournant L, Gazel F, Mody K, Khachtib Y, Roman A, Ursu TM, Zakharov IA, Belcram H, Harry M, Roth M, Simon JC, Oram S, Ricard JM, Agnello A, Beers EH, Engelman J, Balti I, Salhi-Hannachi A, Zhang H, Tu H, Mottet C, Barrès B, Degrave A, Razmjou J, Giraud T, Falque M, Dapena E, Miñarro M, Jardillier L, Deschamps P, Jousselin E, Cornille A (2021) Large-scale geographic survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North Africa. bioRxiv, 2020.12.11.421644, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2020.12.11.421644