Abstract
The increasing amount of genomic data currently available is expanding the horizons of population genetics inference. A wide range of methods have been published allowing to detect and date major changes in population size during the history of species. At the same time, there has been an increasing recognition that population structure can generate genetic data similar to those generated under models of population size change. Recently, Mazet et al. (Heredity 116(4):362–371, 2016) introduced the idea that, for any model of population structure, it is always possible to find a panmictic model with a particular function of population size-change having an identical distribution of \(T_{2}\) (the time of the first coalescence for a sample of size two). This implies that there is an identifiability problem between a panmictic and a structured model when we base our analysis only on \(T_2\). In this paper, based on an analytical study of the rate matrix of the ancestral lineage process, we obtain new theoretical results about the joint distribution of the coalescence times \((T_3,T_2)\) for a sample of three haploid genes in a n-island model with constant size. Even if, for any \(k \ge 2\), it is always possible to find a size-change scenario for a panmictic population such that the marginal distribution of \(T_k\) is exactly the same as in a n-island model with constant population size, we show that the joint distribution of the coalescence times \((T_3,T_2)\) for a sample of three genes contains enough information to distinguish between a panmictic population and a n-island model of constant size.
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Acknowledgements
The authors wish to thank Josué M. Corujo Rodríguez for very interesting discussions in preparing this article. The authors also thank the anonymous reviewers for their reading and for valuable suggestions. This research was funded through the 2015–2016 BiodivERsA COFUND call for research proposals, with the national funders ANR (ANR-16-EBI3-0014), FCT (Biodiversa/0003/2015) and PT-DLR (01LC1617A), under the INFRAGECO (Inference, Fragmentation, Genomics, and Conservation) Project (https://infrageco-biodiversa.org/). The research was also supported by the LABEX entitled TULIP (ANR-10-LABX-41), as well as the Pôle de Recherche et d’Enseignement Suprieur (PRES) and the Région Midi-Pyrénées, France. We finally thank the LIA BEEG-B (Laboratoire International Associé—Bioinformatics, Ecology, Evolution, Genomics and Behaviour) (CNRS) and the PESSOA program for facilitating travel and collaboration between EDB, IMT and INSA in Toulouse and the IGC, in Portugal.
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Appendices
Appendix A Proofs for Sections 2 and 3
Proof of Lemma 1
We first observe that
Then the calculus gives
The intermediate value theorem applied to \(p(\mu )\) thus provides a proof of the result. \(\square \)
Proof of Proposition 2
In order to simplify computations, we make the following change of parameters:
The new parameters a et N verify \(a > 0\) and \(N > 0\) and the matrix Q becomes
The matrix Q has the double eigenvalue 0 and it is easy to check that the corresponding eigenspace is generated by the following non colinear vectors:
We then consider the change of basis matrix
whose inverse is
We have thus obtained a partial diagonalization (by blocks) of the matrix Q:
and we put
The characteristic polynomial of R is the polynomial \(p(\mu )\), which has the following expressions using the new parameters:
which has three strictly negative real roots. These roots are all distinct by Lemma 1.
If \(\mu \) is an eigenvalue of R, we then determine a corresponding eigenvector \(W(\mu )\) by solving the equation \(R W(\mu ) = \mu W(\mu )\).
The computations show that we can choose
We then consider the \(3 \times 3\) passage matrix \(P_2\), whose column vectors are the \(W(\mu _i), \, i=1,2,3\), where the \(\mu _i\) are the three eigenvalues of R:
Some easy computations on the rows show that the determinant of \(P_2\) is a Van der Monde determinant, and hence: \(\mathrm {det}(P_2) = (\mu _1 - \mu _2)(\mu _1-\mu _3)(\mu _2 - \mu _3) \ne 0\).
The computations of the inverse \(P_2^{-1}\) gives
where
with
We further obtain
We then introduce the matrices \(A(\mu )\) and B defined by
where \(\bar{W}_j(\mu )\) (resp. \(\bar{Z}(\mu )\)) is a vector of length 5 obtained by adding two null coordinates to \(W(\mu )\) (resp. \(Z(\mu )\)), and
Emphasizing the rank one property of matrix \(A(\mu )\), let us define the vectors
where \(\mu \) is an eigenvalue of R, and u, v are functions of \(\mu \) defined by
Note that, since
\(\displaystyle -\frac{3M}{n-1}\) and \(\displaystyle -\frac{3(M+2)}{2}\) cannot be eigenvalues and thus \(u \ne 0\) et \(v \ne 0\).
With \(\delta (M,n,\mu ) = 2(n-1)^2 p'(\mu )\), we have
which gives the expression of \(A(\mu )\) in Proposition 2.
The stated result easily follows. \(\square \)
Proof of Proposition 4
Using Eq. (15) and Proposition 2, we deduce that
Note that the matrix \(E_1 E_2^T\) introduced in the proof of Proposition 2 can also be factorized in a different manner. If we define the \(3 \times 3\) matrix C, the \(5 \times 3\) matrix \(D_1\) and the \(3 \times 5\) matrix \(D_2\) by
we may check that, for any value of \(\mu \), we have \(E_1 E_2^T = D_1 C D_2\).
The vectors \(V_1\) and \(V_2\), defined by
verify \(D_2 V_j = 0\) for \(j=1,2\), and hence, using Eq. (25), \(A(\mu )V_j = 0\), for \(j=1,2\).
Therefore, for \(i=1,2,3\),
and the result follows. \(\square \)
Proof of Lemma 2
Note that \(-3\alpha \) and \(-3\beta \), with \(\alpha , \beta \) defined in Eq. (10), are the roots of the polynomial \(q_1(X)= q(X/3)\), where
and on the open subset \(D = \left\{ (n,M):\; n> 2, \; M>0 \right\} \) of \(\mathbb {R}^2\) the polynomials p(X) and \(q_1(X)\) have a common root if and only their resultant \(R(n,M) = \text{ Res }(p(X),q_1(X),X)\) with respect to X is null [see e.g. Lang (2002, Chapter IV–8)].
Because \(R(n,M) = - \frac{M^3}{9(n-1)^2} < 0\) on D, and because the roots \(-3 \alpha \) and \(\mu _3\) are continuous functions of (n, M) on D, the inequality \(-3 \alpha < \mu _3\) for one value of \((n,M) \in D\) implies the inequality everywhere on D. The same is true for the inequality \(\mu _1 < -3 \beta \).
This achieves the proof of the lemma. \(\square \)
Proof of Proposition 5
We will only give the proof of (i), which corresponds to the case of three genes sampled from the same deme. The proofs ot the analogous results (ii) and (iii), corresponding to the two other sample schemes, are similar.
When \(t \rightarrow 0\), using the well-known relation \(P_t = I_5 + tQ + o(t)\), where \(I_5\) denotes the identity matrix, we have the following Taylor expansions:
In particular, we have
Using Eqs. (7)–(11), and a Taylor expansion of order 2 of the exponential in the neighborhood of 0, we easily obtain
When substituting the above expressions into Eq. (11), straightforward calculations give
Further, using Eq. (18), let us denote
We will write a Taylor expansion of order 2 of h(u, t) in the neighborhood of (0, 0). We have \(h(0,0)=0\) and direct computations give
Using the fact that \(P_0 = I_5,\) and \(Q(1,4)=3, Q(1,5)=0\), we obtain
We further compute the second partial derivatives of h in (0, 0). With \(Q^2\) being the square matrix of the rate matrix Q, and using the fact that \(Q^2(1,4) = -9\left( \frac{M}{2}+1\right) \) and \(Q^2(1,5) = \frac{3M}{2},\) we easily derive
The Taylor expansion of order 2 of h(u, t) near (0, 0) finally gives
which finishes the proof. \(\square \)
Proof of Proposition 6
Because \(0< \beta < \alpha \), using Eqs. (7) and (8), we get
and
Therefore, using Eq. (11), we obtain
where \(K_{1,i}(n,M,t)\), given by (20), is strictly positive because \(0< a < 1\) and \(c < 0\).
Using Proposition 2 we get
Therefore, using Eq. (18) and relation \(1 - P_t(i,4) - P_t(i,5) = \sum _{j=1}^3 P_t(i,j)\), we obtain
where
Because \(\frac{\mu _1}{3} < - \beta \) from Lemma 2, we have \( \displaystyle e^{\frac{\mu _1}{3} u} = o(e^{-\beta u}), \) which achieves the proof of (19). \(\square \)
Proof of Proposition 7
We will first prove a useful lemma. \(\square \)
Lemma 3
Let us define \(\phi (\mu )\) by
where the matrix \(A(\mu )\) is given in Proposition 2.
Then,
-
(i)
\(0< \phi (\mu _i)< - \frac{\mu _i}{3} < \alpha , \; i=1,2,3.\)
-
(ii)
Defining h(n) by
$$\begin{aligned} h(n) = \frac{(n-1)\left( 25 - 9n + 5 \sqrt{9n^2 - 18n + 25}\right) }{12 n^2}, \end{aligned}$$we have the following results:
-
(a)
If \(M > h(n)\), then \(\phi (\mu _1)< \beta< \phi (\mu _2)< \phi (\mu _3) < \alpha .\)
-
(b)
If \(M = h(n)\), then \(\phi (\mu _1)< \beta = \phi (\mu _2)< \phi (\mu _3) < \alpha .\)
-
(c)
If \(M < h(n)\), then \(\phi (\mu _1)< \phi (\mu _2)< \beta< \phi (\mu _3) < \alpha .\)
-
(a)
Proof
From Proposition 2 and using \(p(\mu _i)=0\), we get
From Lemma 1, it follows that \(\mu n + 3 >0\). Because \( -\alpha< \displaystyle \frac{\mu _i}{3} < -\beta \) from Lemma 2, we get \(q\left( \frac{\mu _i}{3}\right) < 0\), that proves \(\phi (\mu _i) < - \frac{\mu _i}{3}\).
Now, using again that \(p(\mu _i)=0\), we obtain the following expression for \(\phi (\mu _i)\)
Introducing the new variable \(\nu = \displaystyle \frac{3 M}{2(n-1)\mu + 3nM + 6(n-1)}\), and thus \(\mu = \displaystyle - \frac{3}{2} \frac{(nM + 2n-2))\nu - M}{(n-1) \nu }\), we get that \(\phi (\mu _i)\), for \(i=1,2,3\) are the three real roots of the polynomial
The coefficient signs of r(X) show that r(X) has no negative roots, implying that \(\phi (\mu _i) >0, \; i=1,2,3\), which achieves the proof of (i).
The set of (n, M) such that r(X) and \(q(-X)\) have a common root is obtained by computing their resultant with respect to X, denoted by R(n, M):
In the domain \(D = \{(n,M),\; n>2, \; M>0 \}\) the curve \(6n^2 M^2 + (n-1)(9n-25) M - 6(n-1)^2 = 0\) is identical to the graph of the function \(M = h(n), \; n > 2\).
The set \(D {\setminus } \{(n,h(n)): \; n > 2 \}\) has two connex open components in which the relative position of \(\beta , \alpha \) and \(\phi (\mu _i), \; i=1,2,3\) are the same.
In the component \(D_1 := \{(n,M):\; n>2,\; M > h(n)\}\), one may choose \(n=3, \; M=\frac{4}{3}\) for which
that proves \((ii-a)\).
In the component \(D_2 := \{(n,M):\; n>2,\; M < h(n)\}\), one may choose \(n=3, \; M= \frac{1}{2} \) for which
that proves \((ii-c)\).
The curve arc \(\{(n,h(n)): n > 2 \}\) may be parametrized by
and we obtain
and \((ii-b)\) is proved. \(\square \)
Lemma 3 is now used to prove Proposition 7. First note that we have
for every \(i=1,2,3\).
When \(t \rightarrow + \infty \), \(P_t(i,j) = A(\mu _1)(i,j) e^{\mu _1 t} + o\left( e^{\mu _1 t}\right) ,\; j=1,2\) and thus
Using the definitions of \(F_{2,s}(u)\) and \(F_{2,d}(u)\) in Eqs. (7) and (8), we get
where \(c_1\) and \(c_2\) are given by (23).
On another hand, we have \(P_t(i,j) = A(\mu _1)(i,j) e^{\mu _1 t} + o\left( e^{\mu _1 t}\right) ,\; j=1,2,3\), we obtain
Using the fact that \(1 - P_t(i,4) - P_t(i,5) = \sum _{j=1}^3 P_t(i,j)\), this implies
and thus (21) holds.
It remains to show that \(K_3(n,M,u) >0\).
Using \(c_1 + c_2 = 1\), we may write
From Lemma 2, \(-\alpha< \frac{\mu _1}{3} < -\beta \) and thus \(e^{-\alpha u}< e^{\frac{\mu _1}{3} u} < e^{-\beta u}\). On the other hand, from Lemma 3 we have \(\phi (\mu _1)< \beta < \alpha \). Therefore \(K_3(n,M,u) >0\). \(\square \)
Appendix B The case of \(n=2\) islands
If we now consider the ancestral lineage process for a sample of three genes in the case of a symmetrical n-island model with \(n=2\) two islands, we only have the following four possible configurations:
-
1.
the three lineages are in the same island,
-
2.
two lineages are in the same island and the third one is in the other island,
-
3.
there are only two ancestral lineages left and they are in the same island,
-
4.
there are only two ancestral lineages left and they are in different islands.
The corresponding transition rate matrix is:
The characteristic polynomial of Q is \(\chi _Q(\mu ) = -\mu ^2 p(\mu )\), with
The matrix Q has the double eigenvalue 0 and the corresponding eigenspace of dimension 2 can be generated by the vectors \(\displaystyle \left[ \frac{M}{2},\frac{M}{2}-1, M, -1\right] ^T\) and \(\displaystyle [1,1,1,1]^T\). The two other eigenvalues are \(\mu _1 = - M - 2 + \sqrt{M^2+M+1}\) and \(\mu _2 = - M - 2 - \sqrt{M^2+M+1}\).
An eigenvector for \(\mu _1\) (resp. \(\mu _2\)) is \([3M, 2 \mu _1+3M+6, 0, 0]^T\) (resp. \([3M, 2 \mu _2+3M+6, 0, 0]^T\)), and we may consider the following change of basis matrix P given by
From
and the equality
a proof of the following proposition is obtained.
Proposition 8
The transition kernel \(P_t = e^{t Q}\) is given by
where
with \(\delta (M,\mu ) = 4(\mu + M+2)\) and \(b= \displaystyle \frac{M+2}{2(M+1)}\).
The IICRs \(\lambda _i(\cdot )/3\), for the initial sample configurations \(i=1\) and \(i=2\), correspond to the size-change functions
and the following proposition is verified.
Proposition 9
When \(t \rightarrow \infty \), \(\lambda _i(\cdot ),\; i=1,2\), have the following limit
In Fig. 7 we plot the two functions \(\lambda _i(\cdot ),\; i=1,2\) for \(n=2\) demes and \(M=1\) (left), respectively \(M=0.1\) (right). The dashed line indicates the common asymptotic value \(- \frac{3}{\mu _1}\). We can also show, using Proposition 8, that \(\displaystyle \lim _{M \rightarrow \infty } \lambda _i(t) = 2\) for every \(t > 0\) and \(i=1,2\). This corresponds to the dotted line in the left panel of Fig. 7.
Proof
Using Proposition 8 we get
Then the relations \(3 A(\mu _1)(i,1) = \mu _1 A(\mu _1)(i,3)\) and \(A(\mu _1)(i,2) = \mu _1 A(\mu _1)(i,4)\) allow to prove the result. \(\square \)
The conditional cumulative distribution functions \(\mathbb {P}\left( T_2^{(3),\lambda _i} \le \cdot | T_3^{(3),\lambda _i} = t\right) \) and \(\mathbb {P}_i(T_2^{(3),2,M} \le \cdot | T_3^{(3),2,M} = t) \) are given, for every \(t > 0\), by formulas analogous to (11) and (18):
In order to compare, for \(u, t > 0\), the conditional cumulative distribution functions given in Eqs. (27) and (28), let us introduce the functions
Proposition 10
The functions \(g_i(u,t),\; i=1,2\) have the following asymptotic behaviour:
-
1.
For (u, t) in the neighborhood of (0, 0), we have
$$\begin{aligned} g_1(u,t)= & {} \displaystyle \frac{M}{2} u t + o\left( u^2+t^2\right) , \\ g_2(u,t)= & {} \displaystyle -\frac{u}{3} + \frac{6 M + 1}{18} u^2 + \frac{7 M}{6} u t + o\left( u^2+t^2\right) . \end{aligned}$$ -
2.
For fixed \(t > 0\), when \(u \rightarrow +\infty \),
$$\begin{aligned} g_i(u,t) = - K_{1,i} (M,t) e^{-\beta u} + o(e^{-\beta u}),\; i=1,2, \end{aligned}$$where \(K_{1,i}(M,t) > 0\) is given by
$$\begin{aligned} K_{1,i}(M,t) = \displaystyle \frac{3 P_t(i,1)}{3P_t(i,1) + P_t(i,2)} \frac{1-a}{\beta } - \displaystyle \frac{P_t(i,2)}{3P_t(i,1) + P_t(i,2)} \frac{c}{\beta }, \end{aligned}$$where constants \(\beta , a, c\) are defined in Eqs. (9) and (10) with \(n=2\), i.e.
$$\begin{aligned}&\beta = M + \frac{1}{2}\left( 1 - \left( 4M^2+1\right) ^{1/2}\right) ,\quad a = \frac{1}{2} \left( 1 + \left( 4M^2+1\right) ^{-1/2}\right) ,\\&\quad c = -M \left( 4M^2+1\right) ^{-1/2}. \end{aligned}$$ -
3.
For fixed \(u \ge 0\), we have
$$\begin{aligned} \displaystyle \lim _{t \rightarrow +\infty } g_i(u,t) = -K_3(M,u),\quad i=1,2, \end{aligned}$$where \(K_3(M,u) > 0\) is given by
$$\begin{aligned} K_3(M,u) = c_1 e^{-\beta u} + c_2 e^{-\alpha u} - e^{\frac{\mu _1}{3} u}, \end{aligned}$$with
$$\begin{aligned} \alpha= & {} M + \frac{1}{2}\left( 1 + \left( 4M^2+1\right) ^{1/2}\right) ,\quad \beta = M + \frac{1}{2}\left( 1 - \left( 4M^2+1\right) ^{1/2}\right) ,\; \\ \phi \left( \mu _1\right)= & {} \displaystyle \frac{3M}{2\left( \mu _1 + 3M + 3\right) },\quad c_1 = \frac{\phi \left( \mu _1\right) - \alpha }{\beta -\alpha },\quad c_2 = \frac{\beta - \phi \left( \mu _1\right) }{\beta -\alpha }. \end{aligned}$$
The proof is similar to the one given in the case \(n > 2\).
Most of the calculations of “Appendices A and B” section were made and/or verified using the computer algebra system Maple: programs and tracks of their execution are available from the authors.
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Grusea, S., Rodríguez, W., Pinchon, D. et al. Coalescence times for three genes provide sufficient information to distinguish population structure from population size changes. J. Math. Biol. 78, 189–224 (2019). https://doi.org/10.1007/s00285-018-1272-4
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DOI: https://doi.org/10.1007/s00285-018-1272-4
Keywords
- Inverse instantaneous coalescence rate (IICR)
- Population structure
- Population size change
- Demographic history
- Rate matrix
- Structured coalescent