International Journal of Computational Methods

Abstract Karyotype evolution might fuel speciation and can thereby contribute to species diversity. To test the hypothesis that speciation and karyotype change are linked, we estimated anagenetic and cladogenetic rates of karyotype evolution as well as speciation rates in Orthoptera. We compiled the male diploid chromosome number and the number of visible chromosome arms (the fundamental number) from published sources for 1,541 species. Chromosome-associated speciation rates were estimated by jointly modeling cladogenetic and anagenetic character evolution and the phylogenetic birth-death process in a Bayesian statistical framework using a subset of 516 species from 14 families. Our findings unveiled heterogeneity among orthopteran families in the pace of karyotype evolution and whether it was linked to speciation. In 6/14 clades we found evidence supporting speciation-associated (cladogenetic) karyotype changes, while in 6/14 clades karyotype evolution was primarily anagenetic. The remaining clades (2/14) showed uncertainty in favor of either model. We further analysed whether flightless phenotype, and thus less mobile species, showed higher rates of karyotype evolution. We showed that the flightless phenotype is associated with the rate of chromosome loss. The finding indicates contrasting patterns of karyotype evolution within specific orthopteran lineages, thus emphasizing substantial diversity in the pace of this evolutionary process. It also implies that substantial changes in chromosome number, arising from instances of chromosomal gains and losses, are recurring events in orthopterans that are associated with reproductive isolation and speciation, at least in some groups.

Abstract Inbreeding frequently leads to inbreeding depression, a general reduction in trait values and loss of fitness, and it appears that some sexually selected traits are especially sensitive to inbreeding, but sperm may be an exception. Additionally, because inbreeding depression is always in the direction of low fitness, it can reveal the direction of past selection acting on trait values. Here, we experimentally manipulate levels of inbreeding in a beetle (Tribolium castaneum) by full-sib mating for six generations. This breeding design allowed us to track the effects of increasing homozygosity on male reproductive traits (sperm and testes size), male size and lifespan, and reproductive output within inbred families, and on the heritability of these traits. All traits measured showed significant inbreeding depression and heritabilities tended to increase with inbreeding. Since inbreeding resulted in shorter sperm and smaller testes, it suggests that longer sperm and larger testes confer higher fitness in this beetle.

Abstract Through behavioural adaptation, organisms can alter their environment, and consequently, their exposure to selective pressures. In contrast, physiological traits adapt by accommodating environmental influences. Here, we examine how the coevolution of behavioural and physiological traits is shaped by their different relationships to the environment by modelling the adaptation of species with temperature-dependent sex determination to climate change. In these species, pivotal temperature and maternal nesting behaviour can evolve in response to rising temperatures that destabilise sex ratios. We used individual-based simulation modelling to ascertain the relative response to selection of these traits and determine how temperature-dependent embryonic survival and behavioural plasticity influence their coevolution. We found that pivotal temperature evolved to ameliorate sex-ratio bias more readily than nesting behaviour, though behaviour played an important role in adaptation to extreme environments. Selection favoured increased behavioural evolution when embryonic survival depended on nest temperature, while plasticity reduced the adaptive potential of behaviour. We demonstrate that the capacity of behavioural traits to respond to multiple selective pressures has a substantial impact on the coevolution of behavioural and physiological traits. Our findings highlight the complex interactions that occur when species adapt to new environments and the potential for plasticity to shape the course of evolution.

Abstract Sex chromosomes are theorized to stop recombining and become fixed, yet many taxa show ambiguous genomic signals of sex consistent with either continuous recombination or sex chromosome turnover. Elucidating the basis of sex chromosome conservation or alternatively, turnover, requires comparative studies among natural populations with shared evolutionary histories. The African Great Lake radiations of cichlid fishes display an outstanding propensity to rapidly evolve novel sex-linked regions, yet older cichlid lineages external to these radiations seem to show conservation of a few sex chromosomes. Here, we studied sex-determining regions of species uniquely representing two older lineages within Lake Tanganyika; Oreochromis tanganicae (Oreochromini) and Tylochromis polylepis (Tylochromini). Using a combined SNP- and kmer-based approach, we confirm a ZW system on linkage group (LG) 3 in O. tanganicae, but not the previously proposed sex-determining gene. However, in T. polylepis, no clear region of sex-association could be identified, although kmer-based analyses point towards LG12 as a candidate sex chromosome. Additionally, we investigated four other species from older, non-East African radiation lineages and confirmed LG3 to be frequently associated with sex, but also found stronger signals of sex association on different chromosomes not previously discovered. Combined, these results suggest that homomorphic sex chromosomes are a feature of African cichlids at large. LG3 frequently harbours regions of sex-linkage, but is often polygenic with more strongly sex-linked regions on other chromosomes, possibly denoting its ancestral function as sex-determining across African cichlids, that leaves traces as novel sex-determining regions emerge. Our investigation captures this in a phylogenetic context, from emergence to fixation, or turnover to a new sex chromosome.

Abstract Kin recognition in plants may lead to plastic changes in their behavior, such as altering their floral display size. In this study, we conducted evolutionary simulations of the two floral tactics utilized by plants depending on the genetic relatedness of their neighboring plants. We found that the evolutionary consequences of the floral display size in plants can be classified into four types, based on whether the floral display size increased or decreased in comparison with the case plants disable of kin recognition. As a typical result, the plants that grew with kin behaved altruistically by increasing their floral display size, whereas those that coexisted with strangers behaved selfishly by reducing their floral display size, as is observed in the field. The kin recognition and resultant evolution of the floral display size had the spillover effect on the population scale. Kin recognition generally increased the intraspecific variation in the floral display size and seed production, and decreased the genetic diversity of plant populations.

Abstract Phenotype-environment associations in neonatal animals may arise in wild environments by virtue of ecological dynamics within the nest. Such dynamics may be of special importance to the evolution of temperature-dependent sex determination (TSD), an enigmatic trait which can be adaptive when the incubation temperatures that affect sexual differentiation also have differential effects on fitness of the sexes. To infer causal effects of the nest environment on fitness-relevant phenotypes, we apply structural equation modeling (SEM) to a 14-year dataset of 3085 individual embryos whose position in 179 wild snapping turtle nests could be estimated. We find that temperature has a positive effect on hatchling size, and that the same temperatures that predict hatchling size also predict sex of hatchlings. Further, the probability that embryos develop as males is correlated with hatchling size in the wild, where across all environments, males are slightly and significantly larger than females at hatching. Our SEM reveals that the covariance between size and sex arises because of temperature effects on size, and because of a predictable covariance between egg placement within the nest coupled with maternal effects on egg size. Finally, embryos deep in the nest have a high probability of becoming male even in the hottest years. Our study suggests ecological dynamics occurring within the nest are an interesting and underappreciated source of phenotypic variation. Our study also supports the view that TSD is an adaptive trait, rather than a neutral trait, by showing consistent associations between phenotype and temperature in wild nests of a TSD reptile.

Abstract Investigating the evolution of complex traits in nature requires accurate assessment of their genetic basis. Quantitative genetic (QG) modeling is frequently applied to estimate the additive genetic variance (VA) in traits, combining phenotypic and pedigree data from a sample of individuals. Whether reconstructed from social links or molecular markers, empirical pedigrees differ in completeness, genealogical error rates and other attributes that can impact QG estimation. Here we investigate this impact using human genealogical data for six French-Canadian (FC) populations originating from the same genetic founding source but differing in their pedigrees’ attributes. First, we simulated phenotypic values along pedigrees and under different trait architecture and ‘true’ parameter values (e.g. VA). Then we fitted mixed effects ‘animal’ models to these simulated data, to assess how QG estimation was impacted by pedigree attributes. Our results show that pedigree size and depth were important determinants of the precision, but not accuracy, of genetic parameter estimates. In contrast, pedigree completeness and entropy, two attributes related to the density of genealogical links, were not clearly associated with the performance of parameter estimation. Noticeably, a slight increase in the genealogical error rate was sufficient to cause a detectable underestimation of VA. Including maternal genetic effects into the simulations lead to a slight underestimation of VA with pedigrees of smaller size and depth. Despite originating from the same genetic source, the six pedigrees yielded wide variations in QG estimates under identical conditions. These findings highlight the importance of sensitivity analyses in pedigree-based genetic studies on natural populations.

Abstract Sex allocation theory predicts the adaptive allocation of resources to male versus female reproduction in simultaneous hermaphrodites in response to individual characteristics or environmental factors. Because parasites uptake resources from their hosts, their presence could affect the sex allocation of the hosts. We investigated the effects of infestation status and infestation intensity by the rhizocephalan barnacle Boschmaella japonica on reproduction, including sex allocation, of the host intertidal barnacle Chthamalus challengeri. Feeding activity was also examined as a factor related to resource intake. Both male and female reproductive investment decreased with increasing parasite infestation, and the sex allocation of large infested hosts was more male-biased than that of large uninfested hosts. Moreover, in contrast to the model prediction that male investment does not change under resource limitation, male investment decreased in infested hosts whose resources were taken by parasites. This reduction in male investment could be explained by changes in mating group size, since infested hosts have shorter penises and consequently are able to access fewer mating partners.

Abstract In ovipositing animals, egg placement decisions can be key determinants of offspring survival. One oviposition strategy reported across taxa is laying eggs in clusters. In some species, mothers provision eggs with diffusible defence compounds, such as antimicrobials, raising the possibility of public good benefits arising from egg clustering. Here we report that Drosophila melanogaster females frequently lay eggs in mixed maternity clusters. We tested two hypotheses for potential drivers of this oviposition behaviour: (i) the microbial environment affects fecundity and egg placement in groups of females; (ii) eggs exhibit antimicrobial activity. The results partially supported the first hypothesis. Females reduced egg laying, but did not alter egg clustering, on non-sterile substrates that had been naturally colonised with microbes from the environment. However, oviposition remained unaffected when the substrate community consisted of commensal (fly-associated) microbes. The second hypothesis was not supported. There was no evidence of antimicrobial activity, either in whole eggs or in soluble egg surface material. In conclusion, while we found no behavioural or physiological evidence that egg clustering decisions are shaped by the opportunity to share antimicrobials, females are sensitive to their microbial environment and can adjust egg laying rates accordingly.

Abstract Differences in habitat use impose ecological constraints which in turn lead to functional and morphological differences through adaptation. In fact, a convergent evolutionary pattern is evident when species exhibit similar responses to similar environments. In this study we examine how habitat use influences the evolution of body shape in lizards from the family Lacertidae. We divided our species set into two categories: ground-dwellers and climbers, which encompasses the verticality and horizontality aspects of the habitat. We performed phylogenetic comparative analyses employing 186 species and seven linear morphological traits. Our results show contrasting patterns between head and limb shape, which are considered distinct functional blocks. We observed differences in forelimb proportions, but not in hindlimb length, contrary to what was documented in other lizard groups, demonstrating a novel axis in the limb-locomotion-habitat relationship in this family. In addition, a clear effect of habitat use on head shape was detected. We observed that climbing species present on average flatter heads than ground-dwelling species, as well as different evolutionary trajectories. These findings suggest the complex interplay between habitat use and morphological evolution in lizards, highlighting how distinct selective pressures drive divergent adaptations in different functional traits

Abstract Modularity and developmental (in)stability have the potential to influence phenotype production and, consequently, the evolutionary trajectories of species. Depending on the environmental factors involved and the buffering capacity of an organism, different developmental outcomes are expected. Cactophilic Drosophila species provide an established eco-evolutionary model with well-studied ecological conditions, making them ideal for studying these phenomena. Here, we investigated how variations in larval diet and exposure to alkaloids on primary and secondary host plants affect the degree of integration/modularity and fluctuating asymmetry (FA, a proxy for developmental instability) of wing shape in two sibling species with different degrees of specialisation: Drosophila buzzatii (generalist) and Drosophila koepferae (specialist). Additionally, we compared the anterior–posterior modular configuration with a recently proposed proximal–distal modular configuration. Our results revealed greater independence among proximal–distal modules compared to anterior–posterior modules. Moreover, we observed sex-specific responses, with males exhibiting greater susceptibility to stressful environments than females. Each species showed a particular trait pattern across treatments: D. buzzatii showed increased integration and FA when reared in a nutrient-poor, alkaloid-rich secondary host, while D. koepferae displayed similar responses in novel environments characterised by double doses of alkaloids on the secondary host plant. These findings align with the generalist-specialist paradigm, suggesting that specialists may be challenged by novel environments, whereas generalists may be more affected by stressful conditions. Our study highlights the importance of considering each part of the proximal–distal wing axis independently, and the need to consider ecological-evolutionary history when investigating the relationship between complex phenotypic traits and environmental stress.

Abstract Walnut is a significant woody oil tree species that has been increasingly affected by anthracnose in recent years. Effective anthracnose control is crucial for walnut yield and quality, which requires a comprehensive understanding of the response mechanisms to Colletotrichum gloeosporioides. The PR10/Bet v1-like proteins are involved in defense against various disease, therefore, in this study, 7 JrBet v1s were identified from the walnut transcriptome (named JrBet v1-1~1-7), whose open reading frame (ORF) was 414~483 bp in length with isoelectric point ranging from 4.96 to 6.11. These JrBet v1s were classified into three groups, with the MLP/RRP and Dicot PR-10 subfamilies each comprising three members (the largest ones), indicating that the proteins within these two subfamilies may have evolved from a shared ancestral gene within the broader PR10/Bet v1 protein family. The cis-elements in the promoters of JrBet v1s were involved in response to hormones, coercive, and plant growth metabolism. Most JrBet v1s could be significantly upregulated by walnut anthracnose, JrBet v1-1, JrBet v1-2, JrBet v1-4, and JrBet v1-6 peaked at 12 days of anthracnose stress, showing a 2.85- to 63.12-fold increase compared to the control, while JrBet v1-3, JrBet v1-5 and JrBet v1-7 peaked at 9 days, with a 3.23- to 27.67-fold increase. Furthermore, the significant corelation of the upregulation under anthracnose stress of JrBet v1s and JrChit02-1 as well as JrChit02-2, the genes encoding chitinase, suggesting that during the long process of microevolution in walnut-C. gloeosporioides interactions, walnut has developed a Bet v1-chitinase defense mechanism to counteract pathogen invasion.

Abstract Polymorphic short insertions and deletions (INDELs ≤ 50 bp) are abundant, although less common than single nucleotide polymorphisms (SNPs). Evidence from model organisms shows INDELs to be more strongly influenced by purifying selection than SNPs. Partly for this reason, INDELs are rarely used as markers for demographic processes or to detect divergent selection. Here, we compared INDELs and SNPs in the intertidal snail Littorina saxatilis, focussing on hybrid zones between ecotypes, in order to test the utility of INDELs in the detection of divergent selection. We computed INDEL and SNP site frequency spectra using capture sequencing data. We assessed the impact of divergent selection by analyzing allele frequency clines across habitat boundaries. We also examined the influence of GC-biased gene conversion because it may be confounded with signatures of selection. We show evidence that short INDELs are affected more by purifying selection than SNPs, but part of the observed site frequency spectra difference can be attributed to GC-biased gene conversion. We did not find a difference in the impact of divergent selection between short INDELs and SNPs. Short INDELs and SNPs were similarly distributed across the genome and so are likely to respond to indirect selection in the same way. A few regions likely affected by divergent selection were revealed by INDELs and not by SNPs. Short INDELs can be useful (additional) genetic markers helping to identify genomic regions important for adaptation and population divergence.