Scots pine - panmixia and the elusive signal of genetic adaptation.

Scots pine is the foundation species of diverse forested ecosystems across Eurasia and displays remarkable ecological breadth, occurring in environments ranging from temperate rainforests to arid tundra margins. Such expansive distributions can be favored by various demographic and adaptive processes and the interactions between them. To understand the impact of neutral and selective forces on genetic structure in Scots pine, we conducted range-wide population genetic analyses on 2321 trees from 202 populations using genotyping-by-sequencing, reconstructed the recent demography of the species and examined signals of genetic adaptation. We found a high and uniform genetic diversity across the entire range (global FST 0.048), no increased genetic load in expanding populations and minor impact of the last glacial maximum on historical population sizes. Genetic-environmental associations identified only a handful of single-nucleotide polymorphisms significantly linked to environmental gradients. The results suggest that extensive gene flow is predominantly responsible for the observed genetic patterns in Scots pine. The apparent missing signal of genetic adaptation is likely attributed to the intricate genetic architecture controlling adaptation to multi-dimensional environments. The panmixia metapopulation of Scots pine offers a good study system for further exploration into how genetic adaptation and plasticity evolve under gene flow and changing environment.

Accelerating Adaptation of Forest Trees to Climate Change Using Individual Tree Response Functions.

In forest tree breeding, assisted migration has been proposed to accelerate the adaptive response to climate change. Response functions are currently fitted across multiple populations and environments, enabling selections of the most appropriate seed sources for a specific reforestation site. So far, the approach has been limited to capturing adaptive variation among populations, neglecting tree-to-tree variation residing within a population. Here, we combined the response function methodology with the in-situ breeding approach, utilizing progeny trials of European larch (Larix decidua) across 21 test sites in Austria ranging from Alpine to lowland regions. We quantified intra-population genetic variance and predicted individual genetic performance along a climatic gradient. This approach can be adopted in most breeding and conservation programs, boosting the speed of adaptation under climate change.

Fine-scale spatial genetic structure, mating, and gene dispersal patterns in Parkia biglobosa populations with different levels of habitat fragmentation.

PREMISE: A good understanding of genetic variation and gene dispersal in tree populations is crucial for their sustainable management, particularly in a context of rapid environmental changes. West African Sudanian savannahs are being fragmented and degraded, partly due to expansion of crop cultivation and monocultures that reduce tree density and may impact pollinators. The population dynamics of important indigenous trees could also be affected. We investigated the influence of habitat fragmentation on patterns of genetic diversity and gene dispersal of a key Sudanian agroforestry tree species, Parkia biglobosa. METHODS: Using 10 highly polymorphic nuclear microsatellites, we genotyped 2475 samples from reproductive trees, seedlings, and embryos in four tree populations presenting different levels of habitat fragmentation. RESULTS: Parkia biglobosa presented similar high genetic diversity across the four populations studied. Genetic diversity and inbreeding were similar between adults and embryo cohorts. In all four populations, the selfing rate was less than 1%. The effective number of pollen donors per tree was high (NEP ~ 18-22), as was the pollen immigration rate (from 34 to 74%). Pollen dispersal was characterized by a fat-tailed distribution with mean estimates exceeding 200 m. In three populations, stem diameter had a pronounced effect on male reproductive success. Here, the highest male reproductive success was observed in trees with a diameter at breast height between 60 and 75 cm. CONCLUSIONS: At the scale analyzed, fragmentation does not seem to pose limitations to gene flow in any of the sites investigated, regardless of the landscape configuration associated with the different tree stands. The study provides useful insights on the reproductive biology of an important tree species in the West African savannahs.

In Situ Genetic Evaluation of European Larch Across Climatic Regions Using Marker-Based Pedigree Reconstruction.

Sustainable and efficient forestry in a rapidly changing climate is a daunting task. The sessile nature of trees makes adaptation to climate change challenging; thereby, ecological services and economic potential are under risk. Current long-term and costly gene resources management practices have been primarily directed at a few economically important species and are confined to defined ecological boundaries. Here, we present a novel in situ gene-resource management approach that conserves forest biodiversity and improves productivity and adaptation through utilizing basic forest regeneration installations located across a wide range of environments without reliance on structured tree breeding/conservation methods. We utilized 4,267 25- to 35-year-old European larch trees growing in 21 reforestation installations across four distinct climatic regions in Austria. With the aid of marker-based pedigree reconstruction, we applied multi-trait, multi-site quantitative genetic analyses that enabled the identification of broadly adapted and productive individuals. Height and wood density, proxies to fitness and productivity, yielded in situ heritability estimates of 0.23 ± 0.07 and 0.30 ± 0.07, values similar to those from traditional "structured" pedigrees methods. In addition, individual trees selected with this approach are expected to yield genetic response of 1.1 and 0.7 standard deviations for fitness and productivity attributes, respectively, and be broadly adapted to a range of climatic conditions. Genetic evaluation across broad climatic gradients permitted the delineation of suitable reforestation areas under current and future climates. This simple and resource-efficient management of gene resources is applicable to most tree species.

Crossing borders - European forest reproductive material moving in trade.

Forest reproductive material (FRM) is constantly traded between European countries, but bilateral trade statistics on a European scale are limited. For the first time we analysed national datasets according Council Directiv 1999/105/EC for the tree species Picea abies, Pinus sylvestris, P. pinaster, Fagus sylvatica, Fraxinus excelsior, Quercus robur, Q. rubra, and Q. petraea. Based on the period 2004-2014 we (i) quantified the amount and identified European FRM trade and production routes, (ii) applied a gravity model of economic trade to examine the determinants of trade, (iii) discussed the putative genetic impact of transferred FRM on native tree populations, and (iv) considered legislation and documentation processes to their compliance, purpose, and benefit in producing data relevant to sustainable forest management. On average, 30 million plants and 400,000 kg seeds were annually traded. About 85% of traded seedlings were Norway spruce. Coniferous FRM trade is dominated by Scandinavian and Baltic countries, while broad-leaved species are extensively traded in Central Europe. FRM trade and production are interconnected on a multinational level, and besides domestic FRM, most countries are also trading with foreign material. The results of the gravity model indicate that among other significant factors the bilateral trade is driven by geographical distance, currency, and forestry contribution to the domestic gross product. As no detailed data on seed transfer were made available by most countries, the total FRM transfer is biased and probably underestimated.

Phylogeography of African Locust Bean (Parkia biglobosa) Reveals Genetic Divergence and Spatially Structured Populations in West and Central Africa.

The evolutionary history of African savannah tree species is crucial for the management of their genetic resources. In this study, we investigated the phylogeography of Parkia biglobosa and its modeled distribution under past and present climate conditions. This tree species is very valued and widespread in West Africa, providing edible and medicinal products. A large sample of 1610 individuals from 84 populations, distributed across 12 countries in Western and Central Africa, were genotyped using 8 nuclear microsatellites. Individual-based assignments clearly distinguished 3 genetic clusters, extreme West Africa (EWA), center of West Africa (CWA), and Central Africa (CA). Overall, estimates of genetic diversity were moderate to high, with lower values for populations in EWA (allelic richness after rarefaction [AR] = 6.4, expected heterozygosity [HE] = 0.78, and observed heterozygosity [HO] = 0.7) and CA (AR = 5.9, HE = 0.67, and HO = 0.61) compared with populations in CWA (AR = 7.3, HE = 0.79, and HO = 0.75). The overall population differentiation was found to be moderate (FST = 0.09). A highly significant isolation by distance pattern was detected, with a marked phylogeographic signature suggesting possible effects of past climate and geographic barriers to migration. Modeling the potential distribution of the species showed a contraction during the last glaciations followed by expansion events. The exploratory approximate Bayesian computation conducted suggests a best-supported scenario in which the cluster CWA traced back to the ancestral populations and a first split between EWA and CWA took place about 160000 years before present (BP), then a second split divided CA and CWA, about 100000 years BP. However, our genetic data do not enable us to conclusively distinguish among a few alternative possible scenarios.

Drought Sensitivity of Norway Spruce at the Species' Warmest Fringe: Quantitative and Molecular Analysis Reveals High Genetic Variation Among and Within Provenances.

Norway spruce (Picea abies) is by far the most important timber species in Europe, but its outstanding role in future forests is jeopardized by its high sensitivity to drought. We analyzed drought response of Norway spruce at the warmest fringe of its natural range. Based on a 35-year old provenance experiment we tested for genetic variation among and within seed provenances across consecutively occurring strong drought events using dendroclimatic time series. Moreover, we tested for associations between ≈1,700 variable SNPs and traits related to drought response, wood characteristics and climate-growth relationships. We found significant adaptive genetic variation among provenances originating from the species' Alpine, Central and Southeastern European range. Genetic variation between individuals varied significantly among provenances explaining up to 44% of the phenotypic variation in drought response. Varying phenotypic correlations between drought response and wood traits confirmed differences in selection intensity among seed provenances. Significant associations were found between 29 SNPs and traits related to drought, climate-growth relationships and wood properties which explained between 11 and 43% of trait variation, though 12 of them were due to single individuals having extreme phenotypes of the respective trait. The majority of these SNPs are located within exons of genes and the most important ones are preferentially expressed in cambium and xylem expansion layers. Phenotype-genotype associations were stronger if only provenances with significant quantitative genetic variation in drought response were considered. The present study confirms the high adaptive variation of Norway spruce in Central and Southeastern Europe and demonstrates how quantitative genetic, dendroclimatic and genomic data can be linked to understand the genetic basis of adaptation to climate extremes in trees.

Fourteen simple-sequence repeats newly developed for population genetic studies in Prosopis africana (Fabaceae-Mimosoideae).

BACKGROUND: There is very limited genetic knowledge in Prosopis africana, an important sub-Saharan multi-purpose tree species. Availability of highly polymorphic genetic markers would be helpful for future genetic work. FINDINGS: Leaf samples from 15 trees were used to develop simple sequence repeat (SSR) markers. Size-selected fragments from genomic DNA were enriched for repeats and the library was analyzed on an Illumina MiSeq platform. Fourteen SSRs were selected and applied in two Burkinabe populations (40 adult trees each). The number of alleles varied from 4 to 20, evenness (effective number of alleles/observed number of alleles) averaged to 0.54 and unbiased heterozygosity ranged from 0.305 to 0.925 over all loci and populations. Null alleles were not detected. CONCLUSIONS: Due to the high level of polymorphism and lack of null alleles the developed SSRs can be effectively employed in population genetic studies.

Population Differentiation in Common Walnut (Juglans regia L.) across Major Parts of Its Native Range-Insights from Molecular and Morphometric Data.

Juglans regia is an economically highly important species for fruit and wood production in the warm temperate and subtropical zones of the Northern Hemisphere. Besides the natural influence of climatic and geomorphological barriers, its genetic structure has been strongly modified by humans and the population history is still unclear. For this reason, we investigated mainly natural walnut populations across the Eurasian continent on a molecular (44 populations, 581 trees) and morphometric level (23 populations, 1391 ripe nuts). Population genetic diversity and differentiation were examined by using 7 microsatellite loci. Morphometric characteristics of the nuts (mainly roundness index and nut density) were used to estimate trait variation and population differentiation. Highest allelic richness Rs12 = 7.05 was observed in a Pakistani and the lowest value Rs12 = 3.04 in a Kyrgyz population. The genetic differentiation among populations was high (FST = 0.217; RST = 0.530) indicating a strong phylogeographic pattern. While variation of the roundness index within single populations was high, this trait neither differentiated geographical regions nor was it associated to genetic clusters. Approximated QST based on this trait equalled FST, while approximated QST based on nut density considerably exceeded FST, indicating selection. Nut density was moderately correlated with altitude, latitude, and longitude, and differentiated populations according to their origin. Pakistani and Indian populations showed highest nut densities. These South Asian populations contain putatively ancestral nut forms, which probably have been lost in other populations as a consequence of human selection.

Detection of Self Incompatibility Genotypes in Prunus africana: Characterization, Evolution and Spatial Analysis.

In flowering plants, self-incompatibility is an effective genetic mechanism that prevents self-fertilization. Most Prunus tree species exhibit a homomorphic gametophytic self-incompatibility (GSI) system, in which the pollen phenotype is encoded by its own haploid genome. To date, no identification of S-alleles had been done in Prunus africana, the only member of the genus in Africa. To identify S-RNase alleles and hence determine S-genotypes in African cherry (Prunus africana) from Mabira Forest Reserve, Uganda, primers flanking the first and second intron were designed and these amplified two bands in most individuals. PCR bands on agarose indicated 26 and 8 different S-alleles for second and first intron respectively. Partial or full sequences were obtained for all these fragments. Comparison with published S-RNase data indicated that the amplified products were S-RNase alleles with very high interspecies homology despite the high intraspecific variation. Against expectations for a locus under balancing selection, frequency and spatial distribution of the alleles in a study plot was not random. Implications of the results to breeding efforts in the species are discussed, and mating experiments are strongly suggested to finally prove the functionality of SI in P. africana.

High molecular diversity in the true service tree (Sorbus domestica) despite rareness: data from Europe with special reference to the Austrian occurrence.

BACKGROUND AND AIMS: Sorbus domestica (Rosaceae) is one of the rarest deciduous tree species in Europe and is characterized by a scattered distribution. To date, no large-scale geographic studies on population genetics have been carried out. Therefore, the aims of this study were to infer levels of molecular diversity across the major part of the European distribution of S. domestica and to determine its population differentiation and structure. In addition, spatial genetic structure was examined together with the patterns of historic and recent gene flow between two adjacent populations. METHODS: Leaf or cambium samples were collected from 17 populations covering major parts of the European native range from north-west France to south-east Bulgaria. Seven nuclear microsatellites and one chloroplast minisatellite were examined and analysed using a variety of methods. KEY RESULTS: Allelic richness was unexpectedly high for both markers within populations (mean per locus: 3·868 for nSSR and 1·647 for chloroplast minisatellite). Moreover, there was no evidence of inbreeding (mean Fis = -0·047). The Italian Peninsula was characterized as a geographic region with comparatively high genetic diversity for both genomes. Overall population differentiation was moderate (FST = 0·138) and it was clear that populations formed three groups in Europe, namely France, Mediterranean/Balkan and Austria. Historic gene flow between two local Austrian populations was high and asymmetric, while recent gene flow seemed to be disrupted. CONCLUSIONS: It is concluded that molecular mechanisms such as self-incompatibility and high gene flow distances are responsible for the observed level of allelic richness as well as for population differentiation. However, human influence could have contributed to the present genetic pattern, especially in the Mediterranean region. Comparison of historic and recent gene flow may mirror the progress of habitat fragmentation in eastern Austria.

Conservation priorities for Prunus africana defined with the aid of spatial analysis of genetic data and climatic variables.

Conservation priorities for Prunus africana, a tree species found across Afromontane regions, which is of great commercial interest internationally and of local value for rural communities, were defined with the aid of spatial analyses applied to a set of georeferenced molecular marker data (chloroplast and nuclear microsatellites) from 32 populations in 9 African countries. Two approaches for the selection of priority populations for conservation were used, differing in the way they optimize representation of intra-specific diversity of P. africana across a minimum number of populations. The first method (S1) was aimed at maximizing genetic diversity of the conservation units and their distinctiveness with regard to climatic conditions, the second method (S2) at optimizing representativeness of the genetic diversity found throughout the species' range. Populations in East African countries (especially Kenya and Tanzania) were found to be of great conservation value, as suggested by previous findings. These populations are complemented by those in Madagascar and Cameroon. The combination of the two methods for prioritization led to the identification of a set of 6 priority populations. The potential distribution of P. africana was then modeled based on a dataset of 1,500 georeferenced observations. This enabled an assessment of whether the priority populations identified are exposed to threats from agricultural expansion and climate change, and whether they are located within the boundaries of protected areas. The range of the species has been affected by past climate change and the modeled distribution of P. africana indicates that the species is likely to be negatively affected in future, with an expected decrease in distribution by 2050. Based on these insights, further research at the regional and national scale is recommended, in order to strengthen P. africana conservation efforts.

Dynamic conservation of forest genetic resources in 33 European countries.

Dynamic conservation of forest genetic resources (FGR) means maintaining the genetic diversity of trees within an evolutionary process and allowing generation turnover in the forest. We assessed the network of forests areas managed for the dynamic conservation of FGR (conservation units) across Europe (33 countries). On the basis of information available in the European Information System on FGR (EUFGIS Portal), species distribution maps, and environmental stratification of the continent, we developed ecogeographic indicators, a marginality index, and demographic indicators to assess and monitor forest conservation efforts. The pan-European network has 1967 conservation units, 2737 populations of target trees, and 86 species of target trees. We detected a poor coincidence between FGR conservation and other biodiversity conservation objectives within this network. We identified 2 complementary strategies: a species-oriented strategy in which national conservation networks are specifically designed for key target species and a site-oriented strategy in which multiple-target units include so-called secondary species conserved within a few sites. The network is highly unbalanced in terms of species representation, and 7 key target species are conserved in 60% of the conservation units. We performed specific gap analyses for 11 tree species, including assessment of ecogeographic, demographic, and genetic criteria. For each species, we identified gaps, particularly in the marginal parts of their distribution range, and found multiple redundant conservation units in other areas. The Mediterranean forests and to a lesser extent the boreal forests are underrepresented. Monitoring the conservation efficiency of each unit remains challenging; however, <2% of the conserved populations seem to be at risk of extinction. On the basis of our results, we recommend combining species-oriented and site-oriented strategies.

Divergent pattern of nuclear genetic diversity across the range of the Afromontane Prunus africana mirrors variable climate of African highlands.

BACKGROUND AND AIMS: Afromontane forest ecosystems share a high similarity of plant and animal biodiversity, although they occur mainly on isolated mountain massifs throughout the continent. This resemblance has long provoked questions on former wider distribution of Afromontane forests. In this study Prunus africana (one of the character trees of Afromontane forests) is used as a model for understanding the biogeography of this vegetation zone. METHODS: Thirty natural populations from nine African countries covering a large part of Afromontane regions were analysed using six nuclear microsatellites. Standard population genetic analysis as well as Bayesian and maximum likelihood models were used to infer genetic diversity, population differentiation, barriers to gene flow, and recent and all migration among populations. KEY RESULTS: Prunus africana exhibits strong divergence among five main Afromontane regions: West Africa, East Africa west of the Eastern Rift Valley (ERV), East Africa east of the ERV, southern Africa and Madagascar. The strongest divergence was evident between Madagascar and continental Africa. Populations from West Africa showed high similarity with East African populations west of the ERV, whereas populations east of the ERV are closely related to populations of southern Africa, respectively. CONCLUSIONS: The observed patterns indicate divergent population history across the continent most likely associated to Pleistocene changes in climatic conditions. The high genetic similarity between populations of West Africa with population of East Africa west of the ERV is in agreement with faunistic and floristic patterns and provides further evidence for a historical migration route. Contrasting estimates of recent and historical gene flow indicate a shift of the main barrier to gene flow from the Lake Victoria basin to the ERV, highlighting the dynamic environmental and evolutionary history of the region.

Bioactive constituents in Prunus africana: geographical variation throughout Africa and associations with environmental and genetic parameters.

Prunus africana--an evergreen tree found in Afromontane forests--is used in traditional medicine to cure benign prostate hyperplasia. Different bioactive constituents derived from bark extracts from 20 tree populations sampled throughout the species' natural range in Africa were studied by means of GC-MSD. The average concentration [mg/kgw/w] in increasing order was: lauric acid (18), myristic acid (22), n-docosanol (25), ferulic acid (49), ß-sitostenone (198), ß-sitosterol (490), and ursolic acid (743). The concentrations of many bark constituents were significantly correlated and concentration of n-docosanol was highly significantly correlated with all other analytes. Estimates of variance components revealed the highest variation among populations for ursolic acid (66%) and the lowest for ß-sitosterol (20%). In general, environmental parameters recorded (temperature, precipitation, altitude) for the samples sites were not correlated with the concentration of most constituents; however, concentration of ferulic acid was significantly correlated with annual precipitation. Because the concentration of compounds in bark extracts may be affected by tree size, the diameter of sampled plants at 1.3m tree height (as proxy of age) was recorded. The only relationship with tree diameter was a negative correlation with ursolic acid. Under the assumption that genetically less variable populations have less variable concentrations of bark compounds, correlations between variation parameters of the concentration and the respective genetic composition based on chloroplast and nuclear DNA markers were assessed. Only variation of ß-sitosterol concentration was significantly correlated with haplotypic diversity. The fixation index (F(IS)) was positively correlated with the variation in concentration of ferulic acid. Principal Components Analysis (PCA) indicated a weak geographic pattern. Mantel tests, however, revealed associations between the geographic patterns of bioactive constituents and the phylogenetic relationship among the populations sampled. This suggests an independent evolution of bark metabolism within different phylogeographical lineages, and the molecular phylogeographic pattern is partly reflected in the variation in concentration of bark constituents. The results have important implications for the design of strategies for the sustainable use and conservation of this important African tree species.

Do mites phoretic on elm bark beetles contribute to the transmission of Dutch elm disease?

Dutch elm disease (DED) is a destructive vascular wilt disease of elm (Ulmus) trees caused by the introduced Ascomycete fungus Ophiostoma novo-ulmi. In Europe, this DED pathogen is transmitted by elm bark beetles in the genus Scolytus. These insects carry phoretic mites to new, suitable habitats. The aim of this study was to record and quantify conidia and ascospores of O. novo-ulmi on phoretic mites on the three elm bark beetle species Scolytus multistriatus, Scolytus pygmaeus, and Scolytus scolytus. Spores of O. novo-ulmi were found on four of the ten mite species phoretic on Scolytus spp. These included Elattoma fraxini, Proctolaelaps scolyti, Pseudotarsonemoides eccoptogasteri, and Tarsonemus crassus. All four species had spores attached externally to their body surfaces. However, T. crassus carried most spores within its sporothecae, two paired pocket-like structures adapted for fungal transmission. Individuals of Pr. scolyti also had O. novo-ulmi conidia and ascospores frequently in their digestive system, where they may remain viable. While E. fraxini and P. eccoptogasteri rarely had spores attached to their bodies, large portions of Pr. scolyti and T. crassus carried significant numbers of conidia and/or ascospores of O. novo-ulmi. P. scolyti and T. crassus, which likely are fungivores, may thus contribute to the transmission of O. novo-ulmi, by increasing the spore loads of individual Scolytus beetles during their maturation feeding on twigs of healthy elm trees, enhancing the chance for successful infection with the pathogen. Only S. scolytus, which is the most efficient vector of O. novo-ulmi in Europe, carried high numbers of Pr. scolyti and T. crassus, in contrast to S. multistriatus and S. pygmaeus, which are known as less efficient vectors. The high efficiency of S. scolytus in spreading Dutch elm disease may be partly due to its association with these two mites and the hyperphoretic spores of O. novo-ulmi they carry.

The evolution of invasiveness in garden ants.

It is unclear why some species become successful invaders whilst others fail, and whether invasive success depends on pre-adaptations already present in the native range or on characters evolving de-novo after introduction. Ants are among the worst invasive pests, with Lasius neglectus and its rapid spread through Europe and Asia as the most recent example of a pest ant that may become a global problem. Here, we present the first integrated study on behavior, morphology, population genetics, chemical recognition and parasite load of L. neglectus and its non-invasive sister species L. turcicus. We find that L. neglectus expresses the same supercolonial syndrome as other invasive ants, a social system that is characterized by mating without dispersal and large networks of cooperating nests rather than smaller mutually hostile colonies. We conclude that the invasive success of L. neglectus relies on a combination of parasite-release following introduction and pre-adaptations in mating system, body-size, queen number and recognition efficiency that evolved long before introduction. Our results challenge the notion that supercolonial organization is an inevitable consequence of low genetic variation for chemical recognition cues in small invasive founder populations. We infer that low variation and limited volatility in cuticular hydrocarbon profiles already existed in the native range in combination with low dispersal and a highly viscous population structure. Human transport to relatively disturbed urban areas thus became the decisive factor to induce parasite release, a well established general promoter of invasiveness in non-social animals and plants, but understudied in invasive social insects.

Specificity and transmission mosaic of ant nest-wall fungi.

Mutualism, whereby species interact to their mutual benefit, is extraordinary in a competitive world. To recognize general patterns of origin and maintenance from the plethora of mutualistic associations proves a persisting challenge. The simplest situation is believed to be that of a single mutualist specific to a single host, vertically transmitted from one host generation to the next. We characterized ascomycete fungal associates cultured for nest architecture by the ant subgenera Dendrolasius and Chthonolasius. The ants probably manage their fungal mutualists by protecting them against fungal competitors. The ant subgenera display different ant-to-fungus specificity patterns, one-to-two and many-to-one, and we infer vertical transmission, in the latter case overlaid by horizontal transmission. Possible evolutionary trajectories include a reversal from fungiculture by other Lasius subgenera and inheritance of fungi through life cycle interactions of the ant subgenera. The mosaic indicates how specificity patterns can be shaped by an interplay between host life-cycles and transmission adaptations.