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    Rotating and stacking genes can improve crop resistance durability while potentially selecting highly virulent pathogen strains

    Overview of the model
    This model simulates the population and evolutionary dynamics of different pathogen strains, as they interact with different crop resistant cultivars planted in a single field over successive years. We assume one cultivar is planted each year and we consider a field divided into a finite number m of spatial units (representing limited spaces for infections, or potential lesion sites), in which the spatial aspect is implied rather than explicitly represented. For each year during the cropping season, a number of pathogen spores are released from the infested crop residues, it then lands on the crop plants leading to infections (Fig. 1). These infections are apportioned between the different pathogen strains depending on their previous abundance and interactions with the crop cultivar. At the end of the year, during the non-cropping season, these strains are assumed to sexually recombine in the crop residue. The number of spores released and the number of infections are considered as random variables. We denote these both quantities with an uppercase letter (for example N) in general sense, while their particular realisation or draw in the simulation will be noted with a lowercase letter (for example n). The model was developed using the R Language and Environment for Statistical Computing49.
    Figure 3

    Case 1, model predictions of total infection by each pathogen genotype (proportion of total locations infected, left), and the corresponding frequencies of each virulent allele (right) changing over time under different rotation strategies (From top to bottom: (S1) no rotation; (S2) rotation every year; (S3) rotation every 5 years; and (S4) rotation every year with stacked resistance genes). The parameters are at baseline values: the initial frequency of each virulent allele equals (5%), the fitness modifier is set at 0.9, the modifier of increase rate for non-virulent strains equals 0.05, and the initial amount of inoculum represents (10 %) of available locations.

    Full size image

    Figure 4

    Case 2, model predictions of total infection by each pathogen genotype (proportion of total locations infected, left), and the corresponding frequencies of each virulent allele (right) changing over time under different rotation strategies (from top to bottom: (S1) no rotation; (S2) rotation every year; (S3) rotation every 5 years; and (S4) rotation every year with stacked resistance genes). The initial frequency of each virulent allele equals (50%), and other parameters are at baseline values: the fitness modifier is set at 0.9, the modifier of increase rate for non-virulent strains equals 0.05, and the initial amount of inoculum represents (10 %) of available locations.

    Full size image

    We applied the general model described above to a specific situation with four genes of interaction where there are four different resistance genes that may or may not be deployed within each crop cultivar, and four virulence genes that may or may not be present within each pathogen strain. We assume that the presence of each virulence gene reduces the fitness of a strain independently. Specifically, for each strain i, we define the fitness of that strain (delta _i = delta ^{n_{vir,i}}), where (n_{vir,i}) is the number of virulence alleles present in strain i, and (delta) is a fixed model parameter with potential values between zero and one (Table 1).
    Table 1 Baseline model parameter values used for our analysis, with alternative values shown in parentheses.
    Full size table

    We first set the model parameter values to define a baseline situation where there is a relatively small fitness penalty for virulence alleles (i.e. (delta) is very close to 1, where the value 1 means no penalty); the pathogen has a relatively low ability to reproduce if it does not carry effective virulence genes (i.e. low value for (epsilon), in this baseline situation equal to 0.05); the initial virulence allele frequency (Init.freq) is relatively low, reflecting a low historical selection pressure and lastly the initial quantity of pathogen (Init.path) is also low at (10 %) of carrying capacity (Table 1). We then considered and compared four different strategies for rotating resistant crop cultivars:
    S1.
    No rotation, the same cultivar with only one gene of resistance is employed every year;

    S2.
    A cultivar with a single gene of resistance is employed each year, and the gene of resistance in the cultivar is changed every year, giving a 4-year rotation;

    S3.
    A cultivar with a single gene of resistance is employed each year, and the gene of resistance in the cultivar is changed every 5 years, giving a 20-year rotation; and

    S4.
    A cultivar with two genes of resistance (i.e. pyramided resistance) is employed each year, and the genes of resistance in the cultivar are changed every year, giving a 2-year rotation

    We then investigated how different parameterisations of the model would interact with the selected rotation strategies. We develop four cases in addition to the baseline case described above:
    Case 1.
    Baseline scenario (Table 1).

    Case 2.
    Baseline scenario, except for Init.freq which was increased from 0.05 to 0.5.

    Case 3.
    Baseline scenario, except for Init.freq which was increased from 0.05 to 0.5 and (delta) which was decreased from 0.9 to 0.7.

    Case 4.
    Baseline scenario, except for Init.freq which was increased from 0.05 to 0.5, (delta) which was decreased from 0.9 to 0.7 and (epsilon) which was increased from 0.05 to 0.5.

    Case 5.
    Baseline scenario, except for (epsilon) which was increased from 0.05 to 0.5.

    Genetics
    Cultivar and pathogen strain are both defined through their genotype being restricted to a specific set of interaction genes (loci) related to resistance (for the cultivar) or virulence (for the pathogen). Each gene has two versions (alleles): virulence or avirulence allele for the pathogen and resistance or susceptibility for the cultivar. Virulence and resistance are represented with a 1 and avirulence and susceptibility are represented with a 0 (Fig. 2). If we call ({mathcal {I}}) the set of strains and if (nu) genes of interaction are involved, then the total number of strains will be (left| {mathcal {I}}right| = 2^{nu }). During the infection process, after pathogen spores land on the cultivar, an interaction factor (beta (i,c)) defines the relative rate at which strain i can reproduce within a field of cultivar c, for each strain and cultivar combination (Fig. 2). We consider that a strain overcomes the cultivar genotype when the strain has a virulence allele for every resistance allele of the cultivar (Fig. 2), in which case (beta (i,c)=1), indicating maximum reproduction rate. Otherwise, if the strain does not have a virulence allele for every resistance allele of the cultivar, (beta (i,c)= epsilon), where (epsilon) is a model parameter with constant value (0 le epsilon < 1), indicating a less-than-maximum reproduction rate. As such, (epsilon) is the model parameter modifying the growth and reproduction of pathogen strains not carrying multiple virulence alleles (e.g. 0100) and/or an avirulent pathogen strain (e.g. 0000) (Fig. 2). Accordingly, lower (closer to 0) (epsilon) values represent reduced ability to grow and reproduce in pathogen strains with increasing number of avirulence alleles. Moreover, any strain i with one or more virulence genes is also assumed to suffer a fitness penalty (delta _i) depending on the number of genes involved. Together these interaction factors make a cultivar-strain interaction matrix (B = (beta (i,c))). This code and method for modelling resistance and virulence interactions (without fitness penalty) is similar to those in previous studies48,50. Figure 5 Case 3, model predictions of total infection by each pathogen genotype (proportion of total locations infected, left), and the corresponding frequencies of each virulent allele (right) changing over time under different rotation strategies (from top to bottom: (S1) no rotation; (S2) rotation every year; (S3) rotation every 5 years; and (S4) rotation every year with stacked resistance genes). The fitness modifier is set at 0.7, the initial frequency of each virulent allele equals (50%), and other parameters are at baseline values: the modifier of increase rate for non-virulent strains equals 0.05, and the initial amount of inoculum represents (10 %) of available locations. Full size image Figure 6 Case 4, model predictions of total infection by each pathogen genotype (proportion of total locations infected, left), and the corresponding frequencies of each virulent allele (right) changing over time under different rotation strategies (from top to bottom: (S1) no rotation; (S2) rotation every year; (S3) rotation every 5 years; and (S4) rotation every year with stacked resistance genes). The fitness modifier is set at 0.7, the initial frequency of each virulent allele equals (50%), the modifier of increase rate for non-virulent strains equals 0.5, and other parameters are at baseline values: the initial amount of inoculum represents (10 %) of available locations. Full size image Initial genetic structure of pathogen population At the start of each case, we define the initial proportion of each pathogen genotype using the equation: $$begin{aligned} strains.init = Init.freq^{nr}left( 1-Init.freqright) ^{4-nr} end{aligned}$$ (1) where strains.init is the initial proportion of each pathogen genotype; Init.freq is the frequency of the virulent genes as set by each case and nr is the number of virulent genes present in a given pathogen genotype. We then used a random Poisson distribution generator (rpois function from the stats package in R) to obtain the initial number of spores for each pathogen genotype, where the mean of the Poisson distribution is the proportion of a given pathogen genotype multiplied by the pre-determined pathogen load (Init.path, Table 1). Model dynamics The annual dynamics (Fig. 1) can be divided into two main phases: the phase of parasitic activity, representing events occurring through the cropping season, and the phase of dormancy, representing events occurring between the cropping seasons. During the phase of parasitic activity, the pathogen produces spores which are spread both through the air (sexual ascospores) and via water splash (asexual conidia). These spores may then infect leaves and stems of the cultivar, resulting in new lesions of different strains. During the phase of dormancy, the pathogen remains within the infected crop residue and sexual recombination occurs. These processes are modelled with four steps, three for the parasitic phase and one for the dormancy phase. Figure 7 Case 5, model predictions of total infection by each pathogen genotype (proportion of total locations infected, left), and the corresponding frequencies of each virulent allele (right) changing over time under different rotation strategies (from top to bottom: (S1) no rotation; (S2) rotation every year; (S3) rotation every 5 years; and (S4) rotation every year with stacked resistance genes). The modifier of increase rate for non-virulent strains equals 0.5 and other parameters are at baseline values: the initial frequency of each virulent allele equals (5%), the fitness modifier is set at 0.9, and the initial amount of inoculum represents (10 %) of available locations. Full size image Total amount of spores released First, the model generates the amount of pathogen spores of each strain that is released, using the equation: $$begin{aligned} lambda _{{ released},i}(t) = alpha . n_{{ recombined},i}(t-1) end{aligned}$$ (2) where (lambda _{{ released},i}(t)) represents the expected dispersed propagule (spore) pressure in the field due to strain (i in {mathcal {I}}) during the year t, the parameter (alpha) represents the normal rate of growth for the pathogen from 1 year to the next, and (n_{{ recombined},i}(t-1)) represents the number of spatial units or locations infected by the strain i at the end of the previous year and after genetic recombination. The actual quantity of pathogen strain i released in the current year, (n_{{ released},i}(t)) is then simulated as a Poisson random variable: $$begin{aligned} N_{{ released},i}(t) hookrightarrow {mathcal {P}}(alpha . n_{{ recombined},i}(t-1)) end{aligned}$$ (3) The infective pressure (lambda _{{ infected},i}(t)) is then calculated as: $$begin{aligned} lambda _{{ infected},i}(t) = beta (i,c(t)) . delta _i . n_{{ released},i}(t) end{aligned}$$ (4) where (beta (i,c(t))) is the interaction factor between the strain i and the cultivar c(t) i.e. the cultivar grown in year t, and (delta _i) is the fitness penalty for the particular strain i. Total number of infections Second, the model calculates the total number of infected sites, following a binomial distribution: $$begin{aligned} N_{ infected}(t) hookrightarrow {mathcal {B}}left( m, 1 - prod _{i = 1}^{2^{nu }} (1- rho _i(t))^{n_{{ released},i}(t)}right) end{aligned}$$ (5) where (rho _i(t)) is the probability that a particular given location (among the m possible locations in the field) during year t, will have a given spore from strain i fall down on it and cause a lesion, and thus (displaystyle 1 - prod nolimits _{i = 1}^{2^{nu }} (1- rho _i(t))^{n_{{ released},i}(t)}) represents the probability that at least one of the (displaystyle n_{ released}(t) = sum nolimits _{i = 1}^{2^{nu }} n_{{ released},i}(t)) spores produces a lesion. This equation can be justified in more detail as follows: $$begin{aligned}&P({At; least; one; of; the; n_{ released}(t); spores; produces; a; lesion}) \&quad = 1 - P({ No; released; spores; produces; a; lesion}) \&quad = 1 - prod _{i = 1}^{2^{nu }} P({ A; single; released; spore; of ; strain ; i ; doesn't; produce; a; lesion})^{n_{{ released},i}(t)} \&quad = 1 - prod _{i = 1}^{2^{nu }} (1 - P({A; single; released; spore; of ; strain ; i ; produces; a; lesion}))^{n_{{ released},i}(t)} end{aligned}$$ We assume that a spore will fall on any of the m specific locations with the same probability independently of its infection capabilities. The number of locations m is assumed to be the same for all years whatever the cultivar grown and thus, this probability is independent of the time dimension. Next, we assume that the probability that a spore will induce an infection depends on the interaction factor between the crop cultivar genotype and the pathogen strain (beta (i,c(t))) together with the fitness penalty for that strain (delta _i) . These assumptions mean that: $$begin{aligned} rho _i(t) = P({a; spore; fall; down; on; a; given; location; during ; year; t; and; causes; a; lesion}) \ = P({a; spore; falls; on; a; given; place; where; c(t); is; grown })times \ P({ the; spore; causes; a; lesion} mid { the; spore; falls; on; a; place; where; c(t); is; grown}) \ = frac{1}{m} . beta (i,c(t)) . delta _i end{aligned}$$ Number of infections for each strain Third, the number of infections of each strain is derived from the total number of infections depending on genetic interactions between each strain and crop cultivar being employed that year. Specifically, the total number of infections (N_{ infected}(t) = n_{ infected}(t)) is distributed among the different strains using the multinomial distribution: $$begin{aligned} left( N_{{ infected},1}(t), ldots , N_{{ infected},2^{nu }}(t)right) hookrightarrow {mathcal {M}}left( frac{lambda _{{ infected},1}(t)}{lambda _{ infected}(t)},ldots , frac{lambda _{{ infected},2^{nu }}(t)}{lambda _{{ infected}}(t)}, n_{ infected}(t)right) end{aligned}$$ (6) where (displaystyle lambda _{{ infected}} (t) = sum nolimits _{i = 1}^{2^{nu }} lambda _{{ infected},i}(t)). The number of infected sites due to strain i, without no loss of generalities, follows then the binomial distribution (displaystyle {mathcal {B}}left( n_{ infected}(t),frac{lambda _{{ infected},i}(t)}{lambda _{{ infected}}(t)}right)). Genetic recombination The fourth step involves simulating the process of sexual recombination, where new quantities of each strain are generated based on the previous quantities of each strain. At the end of the year t, we calculate the frequencies (f_j(t)) of each virulent version of each gene from the different genotypes of strains in the crop stubble. We let the genotype of any new spore be represented by a random vector (displaystyle G_i(t) = left( G_{i,1}(t), ldots ,G_{i,nu }(t)right)), where each (G_{i,j}(t)) is a Bernoulli random variable (displaystyle {mathcal {B}}(1,f_j(t))). This vector representation of genotype follows the coding illustrated in (Fig. 2). Assuming that strains recombine independently gene by gene, the probability that (G_i(t)) will be a particular genotype (displaystyle g_i(t) = left( g_{i,1}(t), ldots ,g_{i,nu }(t)right)) is given by: $$begin{aligned} p_i(t) = Pleft( G_i(t) = g_i(t)right) &= prod _{j=1}^{nu } P(G_{i,j}(t) = g_{i,j}(t)) nonumber \ &= prod _{j=1}^{nu } f_j(t)^{g_{i,j}(t)} left( 1 - f_j(t)right) ^{left( 1 - g_{i,j}(t)right) } end{aligned}$$ We can also confirm that across all possible genotypes these probabilities sum to one: $$begin{aligned} sum _{i=1}^{2^{nu }} Pleft( G_i(t) = g_i(t)right) = sum _{i=1}^{2^{nu }} prod _{j=1}^{nu } f_j(t)^{g_{i,j}(t)} left( 1 - f_j(t)right) ^{left( 1 - g_{i,j}(t)right) } = 1 end{aligned}$$ (7) If we shorten the notation for (P(G_i(t) = g_i(t))) to be (p_i(t)) then we can define the recombined version of infected numbers of units of each strain with the following multinomial distribution: $$begin{aligned} left( N_{{ recombined},1}(t), ldots , N_{{ recombined},2^{nu }}(t)right) hookrightarrow {mathcal {M}}left( p_1(t),ldots , p_{2^{nu }}(t), n_{ infected}(t)right) end{aligned}$$ (8) Poisson, binomial and multinomial distribution In plant pathology, it is often relevant to model infections by a random variable. Let’s imagine a released spore flying in the air, we can say that this spore will land on a specific leaf and infect it with a given probability p, then it won’t with probability (1 - p) because these are the only two possible events. We can define Y a random variable to model the situation. If we say the event ({Y = 1}) represents the success of the event (landing and infection) and ({Y = 0}) represents the failure, with this definition we say that Y follows a Bernoulli distribution. The values attributed to the variable depending on the events allow the following generalisation: If we consider n spores, each of them realizing an infection on a specific plant area they fell on with the same probability p, then we can associate to each spore a Bernoulli distribution (Y_i) where (i in {1,ldots ,n }). If we are interested in the total number of infections occurring on this leaf, assuming the fact that they will happen independently of each other, we can model this situation by the variable (displaystyle S = sum nolimits _{i = 1}^n{Y_i}), called binomial variable. We can also denote briefly (S hookrightarrow {mathcal {B}}(n,p)), where n represents the number of events and p the probability of success of each event. Moreover, the Bernoulli variable Y is related to binomial distribution in the way that we can write (Y hookrightarrow {mathcal {B}}(1,p))51,52. Usually it is more likely to model such events by a Poisson law rather than binomial law53,54. When the number of events is so big that we can approximate it by infinity, and when the probability of success of each event is very small, close to zero, it is possible to link both Poisson and binomial distribution through their respective expectations. So if (lim nolimits _{begin{array}{c} n nearrow +infty \ p searrow 0 end{array}} n*p = lambda ,) then if we define (X hookrightarrow {mathcal {P}}(lambda )), we have (S xrightarrow {text {distribution}} X). Returning to our example, that means that if we have a ‘close to infinity’ number of spores that could fall onto a given plant and infect it with a very small probability p for each of them and still acting independently, we can model the total number of infections by both S or X. Even if there are millions and millions of spores released, this amount is still small compared to infinity, so using X is still a modelling approximation. The use of binomial or Poisson laws depends on the complexity of the situation. For example, if the modeller wants to simulate a model where he anticipates 15 infections, they can use (X hookrightarrow {mathcal {P}}(15)) or (S hookrightarrow {mathcal {B}}(10000,0.0015)) or (S hookrightarrow {mathcal {B}}(1000000,0.000015)). We consider now a situation where the plant is attacked by a big number of spores, but with different genotypes modifying their ability to infect, some strains being more efficient than others. To model this situation, we can use a vector of variables, each component representing the number of successes due to a specific genotype. We can choose a vector of binomial number or Poisson number. If we consider the case of a threshold in terms of available space to be infected (a maximum number of infections for the plant), such that spores of different strains are competing for those places, we suggest using a vector of random numbers that follows a multinomial law. This distribution derives from the binomial law, although each component is a specified binomial distribution defined from the parameters of the multinomial distribution. But, it is still possible to interpret some of these components via a conditional Poisson distribution. From binomial to multinomial distribution The binomial distribution is a particular case of the multinomial distribution. We consider S a binomial distribution of parameters (n, p) counting the number of success of n independent events where the basic probability of success is p. Let U the random variable be defined by (n-S) the number of failures. In the case where S represents the number of infections, U represents the number of uninfected places. The probability to get k infections is given by: $$begin{aligned} P(S = k) = {n atopwithdelims ()k} p^k (1-p)^{n-k} = {n atopwithdelims ()n-k} p^k (1-p)^{n-k} = P(U = n-k) end{aligned}$$ (9) As a result, the probability of having k success is the same that having (n-k) failures. Then the Eq. (9) shows that U follows a binomial distribution with parameters ((n, 1-p)). We can also say that the couple (S, U) follows a multinomial distribution of parameter ((p, 1-p, n)), that we can denote ((S,U) hookrightarrow {mathcal {M}}(p, 1-p, n)). In a more general way, the analogue of the binomial distribution is the multinomial distribution, where each trial results in exactly one of some fixed finite number k possible successes, with probabilities (p_1), ..., (p_k) (so that (p_ige 0) for i = 1, ..., k and (sum nolimits _{i=1}^k p_i = 1)), and there are n independent trials. Then if the random variables (X_i) indicate the number of times outcome number i is observed over the n trials, the vector (X = (X_1, ldots , X_k)) follows a multinomial distribution with parameters n and p, where (p = (p_1, ldots , p_k)), that we can also write ({mathcal {M}}left( p_1,ldots ,p_n, N = kright))55. From Poisson to multinomial distribution We consider here a total number of successes (meaning in our example a number of spores that fall on a place and infect it) X being the sum of the infections due to (omega) different strains (X_i) ((1le i le omega)). If we consider that each (X_i) follows a Poisson law of parameter (lambda _i) and that they are all independent, then X follows a Poisson law of parameter (displaystyle lambda = sum nolimits _{i=1}^{omega } lambda _i). The distribution of each (X_i) conditionally to (X = n) is a binomial distribution ({mathcal {B}}(n,frac{lambda _i}{lambda })). We can prove it for all variable (X_j), with (j in {1,ldots ,omega }): $$begin{aligned} Pleft( X_j = k left| right. sum _{i=1}^{omega } X_i = n right) &= frac{P left( X_j = k,displaystyle sum nolimits _{begin{array}{c} i = 1 \ ine j end{array}}^{omega } X_i = n-k right) }{P left( displaystyle sum nolimits _{i = 1}^{omega } X_i = n right) } \ &= frac{Pleft( X_j = k right) Pleft( displaystyle sum nolimits _{begin{array}{c} i = 1 \ i ne j end{array}}^{omega } X_i = n-k right) }{P left( displaystyle sum nolimits _{i = 1}^{omega } X_i = n right) } end{aligned}$$ that we obtain using the Bayes formula for conditioning and the use of independence between the (X_i)’s. Then we replace the probabilities by their Poisson values: $$begin{aligned} Pleft( X_j = k left| right. sum _{i = 1}^{omega } X_i = n right) &= frac{e^{-lambda _j}{lambda _j}^k}{k!} frac{e^{- displaystyle sum nolimits _{begin{array}{c} i = 1 \ ine j end{array}}^{omega } lambda _i}{left( displaystyle sum nolimits _{begin{array}{c} i = 1 \ ine j end{array}}^{omega } lambda _i right) }^{n-k}}{(n-k)!} frac{n!}{e^{-displaystyle sum nolimits _{i = 1}^{omega } lambda _i}{left( displaystyle sum nolimits _{i = 1}^n lambda _i right) }^{omega }} \ &= {n atopwithdelims ()k} frac{{lambda _j}^k {left( displaystyle sum nolimits _{begin{array}{c} i = 1 \ ine j end{array}}^{omega } lambda _i right) }^{n-k}}{{left( displaystyle sum nolimits _{i = 1}^{omega } lambda _i right) }^n} = {n atopwithdelims ()k}{left( frac{lambda _j}{displaystyle sum nolimits _{i = 1}^{omega } lambda _i}right) }^k {left( frac{displaystyle sum nolimits _{begin{array}{c} i = 1 \ ine j end{array}}^{omega } lambda _i}{displaystyle sum nolimits _{i = 1}^{omega } lambda _i}right) }^{n-k} end{aligned}$$ Generalizing this result to the random vector of the (displaystyle (X_i)_{1 le ile omega }) for (omega) strains, the distribution of this vector conditionally to the total number X is a multinomial distribution ({mathcal {M}}left( frac{lambda _1}{lambda },ldots ,frac{lambda _n}{lambda }, X = nright))55. Properties of the model Let (X_1),..., (X_{2^{nu }}) independent random variables such that (X_j hookrightarrow {mathcal {P}}(lambda _{{ infected},j}(t))) for all (j in {1,ldots ,2^{nu }}), we have the following results: A. When (m rightarrow infty), (displaystyle N_{ infected}(t) hookrightarrow {mathcal {P}}(sum nolimits _{j=1}^{2^{nu }} lambda _{{ infected},j}(t))), B. For all (j in {1,ldots ,2^{nu }}), (displaystyle N_{ infected, j}(t) xrightarrow {text {distribution}} X_j left| right. sum nolimits _{i = 1}^{2^{nu }} X_i = n), C. With A and B when (m rightarrow infty), it is equivalent to either simulate (N_{ infected}(t)) then the conditional multinomial vector (displaystyle left( N_{{ infected},1}(t), ldots , N_{{ infected},2^{nu }}(t)right)) conditionally to the realisation (n_{ infected}(t)), or to simulate directly the previously defined variables (X_1),..., (X_{2^{nu }}). The number of infected sites due to strain j, without any loss of generalities, follows the binomial distribution (displaystyle {mathcal {B}}left( n_{ infected}(t),frac{lambda _{{ infected},j}(t)}{lambda _{{ infected}}(t)}right)). It is important to notice that it is the same law as a Poisson variable with parameter (lambda _{{ infected},j}(t)) conditionally to the realisation (n_{ infected}(t)) of a Poisson variable with parameter (lambda _{{ infected}}(t)). Referring to formula (10), we can see that when the number of sites available for infection goes towards infinity, meaning that (N_{{ infected}}(t)) behaves like a Poisson law of parameter (sum nolimits _{i = 1}^{2^{nu }} lambda _{{ infected},i}(t)), then the variables (displaystyle left( N_{{ infected},i}(t)right) _{1 le i le 2^{nu }}) behave like independent Poisson law of respective rates (displaystyle left( lambda _{{ infected},i}(t)right) _{1 le i le 2^{nu }}). Proof of the properties of the model A. With the help of the reminder, we just have to prove this result: $$begin{aligned} lim _{m rightarrow infty } Eleft( N_{ infected}(t)right) = sum _{i=1}^{2^{nu }} lambda _{{ infected},i}(t), end{aligned}$$ (10) which could be obtained with the mean value theorem56. It means that if the total number of places available for infections was unlimited, these infections could be regarded as being Poisson distributed, with infection pressure as defined previously. We consider the notation of (5), and to simplify the formula we will note: (rho _i = frac{1}{m} . beta _i) and because the result (10) does not depend on time we reduce the notation such that (10) is equivalent to: $$begin{aligned} lim _{m rightarrow infty } Eleft( N_{ infected}right) = sum _{i=1}^{2^{nu }} lambda _{{ infected}, i}, end{aligned}$$ (11) and then we want to prove that: $$begin{aligned} lim _{m rightarrow infty } m . left( 1 - prod _{i=1}^{2^{nu }} left( 1- frac{beta _i}{m}right) ^{n_{{ released},i}}right) = sum _{i=1}^{2^{nu }} lambda _{{ infected}, i} end{aligned}$$ (12) Replacing m by (frac{1}{x}), with (xne 0), the latest equation equals: $$begin{aligned} lim _{x rightarrow 0} frac{1}{x}. left( 1 - prod _{i=1}^{2^{nu }} (1- xbeta _i)^{n_{{ released},i}}right) = sum _{i=1}^{2^{nu }} lambda _{{ infected}, i} end{aligned}$$ (13) We define (displaystyle f_{beta , n_{released}}(x) = prod _{i=1}^{2^{nu }} f_{i,({beta , n_{released}})}(x) = prod _{i=1}^{2^{nu }} (1 - xbeta _i)^{n_{{ released},i}}). Taking into account the fact that $$begin{aligned} f_{beta , n_{released}}'(x) = left( prod _{i=1}^{2^{nu }} f_{i,({beta , n_{released}})}(x)right) ' = sum _{i=1}^{2^{nu }} left[ f_{i,({beta , n_{released}})}'(x) prod _{begin{array}{c} i=1 \ jne i end{array}}^{2^{nu }}f_{j,({beta , n_{released}})}(x)right] , end{aligned}$$ (14) we apply the mean value theorem (56) to the derivable function (f_{beta , n_{released}}), we got the following result: $$begin{aligned} lim _{x rightarrow 0} frac{left( 1 - f_{beta , n_{released}}(x)right) }{x} &= - lim _{x rightarrow 0} frac{left( f_{beta , n_{released}}(0) - f_{beta , n_{released}}(x)right) }{0 - x} nonumber \ &= -left( f_{beta , n_{released}}'(0)right) = sum _{i=1}^{2^{nu }} beta _i n_{released, i} end{aligned}$$ (15) that finishes the proof of point A. B. The result is immediate knowing the upper reminder concerning the Poisson–Multinomial laws relationship. We just have to take the value of (omega = 2^{nu }). C. When m is close to infinity, (N_{ infected}(t)) follows a Poisson distribution whose parameter (expectation) is a sum of parameters. A property of Poisson distribution is that the law of a sum equals in distribution the sum of independent Poisson variables with the respective terms. So that we can rewrite B: For all (j in {1,ldots ,2^{nu }}), (displaystyle N_{ infected, j}(t) xrightarrow {text {distribution}} X_j left| right. N_{ infected}(t) = n). More

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    Researchers using environmental DNA must engage ethically with Indigenous communities

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    A birdstrike risk assessment model and its application at Ordos Airport, China

    Study area and data survey method
    Ordos Civil Aviation Airport, our study site, is located in the southwestern part of the Inner Mongolia Autonomous Region, China. It is characterized by mid-temperate continental climate and is located on the northeastern edge of the Mu Us Desert. Its main characteristics are a long winter and short summer, but has four distinct seasons. The mean annual temperature is 6.2 ℃, and the mean annual precipitation is 358 mm, mostly concentrated between June and August. The mean annual wind speed is 3.6 m/s17. There are five main land cover types in Ordos civil aviation airport and its surrounding areas: farmland, residential areas, woodland, shrub grassland and wetland.
    We used the line transects method and point counts method to investigate the environment and birds within our study area. It is a commonly used bird survey method, and is also widely used in the survey of birds in and around airports. The line transects were 1000 m × 100 m and the walking speed was 1.5–2.0 km/h. We observed and recorded birds with 10 × 50BA and 30 × 77BA Leica telescopes, SLR digital cameras (Canon 5D Mark III) with telephoto lenses (Canon 100–400 mm). The point count method we used had an observation radius of 200 m. We observed birds with 10 × 50BA Leica binoculars and a 30 × 77BA Leica fixed-mount spotting scope18,19,20,21,22. The flight altitude was estimated using a visual comparison method: an altimeter was used to measure the height of trees and buildings in the observation area and these heights were used to estimate the flight altitude of observed birds. Bird identifications were based on A Field Guide to the Birds of China23.
    The survey areas were divided into three areas: A, B and C. Section A was located within the boundary of the airport. Section A surveys consisted of five shrub grassland transects, with one transect on the runway and one on the apron. Section B was the area within 4 km of the center of the airport (but excluding Section A). There were five woodlands, nine shrub grassland, two farmland and four residential areas. Section C consisted of all areas located with 8 km of the center of the airport, excluding Sections A and B. In Section C we established three woodlands transects, three shrub-grassland transects, two farmland transects and four wetland transects. The species, quantity, distribution, cluster and flight altitude of birds in 39 transects or point counts set up within 8 km of the airport and its surrounding areas were investigated monthly by the method of sample strip or sample point (wetland using sample point method). A total of 468 individual point count or transect surveys were conducted over the study year.
    Birdstrike risk assessment model
    Investigating the bird situation in the airport and surrounding areas is a prerequisite for birdstrike prevention. The establishment of a scientific and standardized risk assessment process for birdstrike prevention (Fig. 2) is helpful for the systematic evaluation of birdstrike risk. This model is based on the ISO 31000 risk management process24—risk identification, risk analysis, risk assessment, risk response, risk recording and reporting, communication and consultation, monitoring and review. A flow chart for bird strike risk assessment was constructed.
    Figure 2

    Flow chart of the airport birdstrike risk assessment process.

    Full size image

    The occurrence of a birdstrike is a matter of probability. The consequences of a birdstrike are a matter of severity, with loss of aircraft or life occurring in extreme cases. Together they combine to determine birdstrike risk, and thus our five risk factors are meant to capture severity and likelihood. The first risk factor is the comparative number, which is important for the simple reason that if a bird species collides with an airplane, a greater number of birds have more serious consequences for an airplane. Among the bird strike events between 2007 and 2014 with the largest record impact energy, half of them involved species in the family Anatidae, and they were all birds with a relatively large comparative number25,26. The second risk factor is bird weight. The greater the weight of a bird, the greater the force generated by an aircraft impact, and the severity of birdstrikes will also increase. Flight altitude is an important factor in the analysis of birdstrike risk12. According to ICAO data, we use 40 m as the critical value of the risk zone. If the average flight height of a bird species is closer to the critical value, the risk of birdstrike will be higher12. Our fourth risk factor is a clustering coefficient, which relates to the living habits of a bird species to move in large groups. If a bird species often gather in large numbers, then the possibility of encountering an aircraft and causing a birdstrike event is greater. This is due to the nature of the collective behavior of birds while flying in flocks of murmurations. Following large, tight formations, birds make fewer independent moving decisions, being forced to constantly react to the movements of their neighbors and having their view partially obscured. They may not have space to avoid oncoming aircraft, or may lack the freedom and alert to choose a successful escape path leading to a higher probability of collision with the aircraft27,28. About 80% of birdstrikes occur during the take-off, climb, approach, and landing phases of flights12,13,29,30, so the distance between bird activity from the flight zone is also an important factor in assessing the probability of birdstrikes. Combining with the above analyses, a risk assessment matrix based on the five factors of bird number, weight, flight altitude, cluster coefficient and range of activity was proposed to assess the risk level of bird species in the airport and its surrounding area within 8 km.
    Risk factor assignment
    1.
    Comparative number = (the number of individual birds/the number of individuals with the most number of birds) × 100.

    2.
    Comparative weight = (estimated weight of all birds of a single species/the largest weight of all birds of any species) × 100.

    3.
    Risk coefficient of flight height:

    Flight height H (m)
    Risk coefficient of flight height
    H  > 100
    0.1
    100 ≥ H  > 50
    0.5
    50 ≥ H  > 30
    1
    30 ≥ H  > 5
    0.5
    5 ≥ H
    0.1

    4.
    Clustering coefficient assignment:

    Number of individuals of a cluster
    Cluster coefficient
    N  > 100
    1
    100  > N ≥ 20
    0.5
    20  > N ≥ 3
    0.2
    3  > N ≥ 1
    0

    5.
    Activity range risk coefficient assignment: according to the bird species observed area, it could be divided into three levels: activities in flight area, activities within 4 km from flight area, activities within 8 km from flight area but not within 4 km. If a bird species has activity in each area, the nearest one to the flight zone will be used as the input for the risk assessment model. The birds distributed in these three regions were assigned 0.9, 0.6 and 0.3 respectively.

    Risk assessment matrix

    $$ {text{Likelihood }} = , left( {{text{cluster coefficient }} + {text{ Risk coefficient of flight height }} + {text{ Activity range risk coefficient}}} right) , times { 1}00 , /{ 3} $$

    $$ {text{Severity }} = , left( {{text{comparative number }} + {text{ comparative weight}}} right) , times { 1}00/{2} $$

    The expert evaluation method is used to determine the numerical range31 (Table 1).
    Table 1 Birdstrike likelihood and severity rating.
    Full size table

    According to the very low, low, moderate, high and very high levels of possibility and severity (Table 1), the level of potential threatening birds are divided into three risk levels: high danger (level 3), moderate danger (level 2), and low danger (level 1). (Table 2).
    Table 2 Airport birdstrike risk assessment matrix.
    Full size table

    Adjust the risk level of individual bird species according to the actual situation of the airport:
    1.
    If the bird is a raptor, increase the risk level by one.

    2.
    The risk level for bird species that are seen crossing a runway or passing through the sky above the runway more than three times should be increased by one.

    Raptors fly fast, and collisions with airplanes can have very serious consequences. Among the birdstrike events with the largest record of birdstrike impact energy from 2007 to 2014, half of them were raptors. However, because their weight is actually low compared to birds like ducks, and their solitary habits, the risk level calculated by this method is often lower than the actual risk, so the risk level of the raptor is increased by one level. Most birdstrikes occur when the aircraft takes off and lands. If the bird’s movement often crosses the runway or the nearby sky, it is more likely to cross an aircraft’s flight trajectory, and therefore is very dangerous for the aircraft. For this reason, when a bird species is seen crossing the runway and flying over the top of the runway three times, the risk level of that species should be increased by one.
    Each airport should adjust their assessments based on locally collected empirical data on strike likelihood and severity as well as ongoing bird monitoring at the airport and its surrounding environment. More

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    The experimental design and fish use protocol were approved by the Institutional Animal Care and Use Committee (IACUC) of Dartmouth College. Also, we conducted all experiments in accordance with relevant guidelines and regulations. We euthanized the fish by single cranial pithing in the nutritional feeding experiment.
    Diet formulation for nutritional feeding experiment
    We incorporated N. oculata defatted biomass to replace different percentages of FM and whole cell Schizochytrium sp. to replace all FO in three tilapia experimental diets for a nutritional feeding trial. These three diet formulations were based on our previous digestibility data for N. oculata defatted biomass and whole cell Schizochytrium sp.17,30,33, and a prior study showing potential to replace all FO with whole cell Schizyochytrium sp.30. We compared these three experimental diets to a reference diet (served as control diet) containing FMFO at levels found in commercial tilapia feed. All diets were iso-nitrogenous (37% crude protein) and iso-energetic (12 kJ/g). Microalgae inclusion diets used N. oculata defatted biomass to replace 33% (33NS), 66% (66NS), and 100% (100NS) of the FM and whole cell Schizochytrium sp. to replace all FO in the test diets (33NS, 66NS, 100NS). Thus N. oculata comprised 3%, 5% and 8% of the diet by weight, respectively, and Schizochytrium sp. made up 3.2% of the diet by weight. We produced the diets in accordance with our previous work17,30,36. We obtained dried Schizochytrium sp. from ALGAMAC, Aquafauna Bio-marine, Inc., Hawthorne, CA, USA; and menhaden FO from Double Liquid Feed Service, Inc., Danville, IL, USA. Qualitas Health Inc., which markets EPA-rich oil extracted from N. oculata as a human supplement39 and seeks uses for tons of under-utilized defatted biomass from its large-scale production facilities, donated the N. oculata defatted biomass. Supplementary Table S8 reports proximate compositions and amino acid profiles of N. oculata defatted biomass and Schizochytrium sp.; total fatty acid profile by percentage of the defatted biomass and Schizochytrium sp ingredients reported in Supplementary Table S9; and macromineral and trace element composition of both ingredients reported in Supplementary Table S10. The formula, proximate analysis, and amino acid profiles of four dietary treatments reported in Table 1. The fatty acid profiles reported in Supplementary Table S11 and the macrominerals and trace elements of the four experimental diets reported in Supplementary Table S7.
    Table 1 Formulation (g/100 g diet) and essential amino acids (% in the weight of diet) of four experimental diets for juvenile tilapia.
    Full size table

    Experimental design and sampling to evaluate tilapia growth on N. oculata defatted biomass and Schizochytrium sp. Diets
    We conducted the feeding experiment using a completely randomized design of four diets × three replicates tanks in recirculating aquaculture systems (RAS). Four hundred eighty Nile tilapia (mean initial weight 34.5 ± 2.06 g) were put into randomized groups of 40, bulk weighed, and transferred to a tank. Tilapia had been acclimated to the FMFO containing reference diet for 7 days prior to distribution. The initial stocking density remained within levels recommended to avoid physiological stress on tilapia ( More

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