Turnover and accumulation of genetic diversity across large time-scale cycles of isolation and connection of populations

Abstract

Major climatic and geological events but also population history (secondary contacts) have generated cycles of population isolation and connection of long and short periods. Recent empirical and theoretical studies suggest that fast evolutionary processes might be triggered by such events, as commonly illustrated in ecology by the adaptive radiation of cichlid fishes (isolation and reconnection of lakes and watersheds) and in epidemiology by the fast adaptation of the influenza virus (isolation and reconnection in hosts). We test whether cyclic population isolation and connection provide the raw material (standing genetic variation) for species evolution and diversification. Our analytical results demonstrate that population isolation and connection can provide, to populations, a high excess of genetic diversity compared with what is expected at equilibrium. This excess is either cyclic (high allele turnover) or cumulates with time depending on the duration of the isolation and the connection periods and the mutation rate. We show that diversification rates of animal clades are associated with specific periods of climatic cycles in the Quaternary. We finally discuss the importance of our results for macroevolutionary patterns and for the inference of population history from genomic data.

Keywords: diversification; migration; population subdivision; secondary contact.

Figure 1.

Trajectories of within- (h_s) and between-population (h_b) genetic diversities under cycles of isolation and connection: (a) in the long-period domain P > P_I and (b) in the short-period domain P < P_W. The dashed and dotted lines represent the expected equilibrium value when populations are connected and isolated, respectively. In (a), both h_s and h_b reach their expected equilibrium value at the end of each connection and isolation period. In (b), both h_s and h_b tend to their equilibrium value of connection (dashed line) with very small fluctuations. Parameters are M = 40, n = 10, N = 2 000, μ = 2.5 × 10⁻⁵. (a) P = 60 000, (b) P = 150.

Figure 2.

Trajectories of within- (h_s) and between-population (h_b) genetic diversities under cycles of isolation and connection in the domain P_W < P < P_I when initial genetic diversity h_b(0) is (a) low and (b) high. In (a), when h_b(0) is low, the successive peaks of within-population genetic diversity (grey arrows) increase in size, while in (b) they decrease in size. In both (a) and (b), the equilibrium trajectories of genetic diversity (framed by a rectangle) are the same. Parameters are M = 400, θ = 0.1 n = 4, N = 10 000, P = 50 000 generations.

Figure 3.

(a) Turnover and (b) accumulation of within-population genetic diversity h_s during cycles of isolation and connection, as a function of the period P and the scaled mutation rate 4Nμ, (c) domains of turnover and accumulation of h_s, (d) relationship between P and the net diversification rate of clades from the major animal orders. Turnover of h_s is measured as the amplitude of the variations of h_s within a cycle. Accumulation of h_s is measured as the mean excess of h_s per generation compared to its expected equilibrium value. In (c), Domain A presents large turnover of h_s. Domain B presents both turnover and accumulation of h_s. Domain C presents small turnover and large accumulation of h_s. In domain D, h_s saturates and all h_s values are larger than 0.9 during the cycles. Parameters in (a–c) are n = 10 populations, m = 0.01 , 2N = 1000 for each population, 200 000 generations. (d) P and net diversification rate for species representative of the main animal orders: mammals (Muridae, Ursidae, Bovidae, Cervidae, Hystricidae, Cercopithecidae, Cebidae, Cricetidae [42]), birds (passerines, [43], Darwin's finches, [44]), reptiles (collubrid snakes, [42], annoline lizards, [45]), bony fishes (Ictalurus, Cyprinidae, [42], cichlids, [46]), insects (Tipulidae, Formicinae [42]), bivalves (Petricolidae, Mesodematidae, Semelidae [42]), barnacles [42] and echinoids (Mellitidae, Clypeasteridae, Laganidae [42]). P corresponds to the period of climatic cycles in generations (100 000 years cycles divided by the generation time of each species). The shaded area represents the range of diversification rates, computed in sliding windows of 0.2 log₁₀(years) (see alternative window sizes in the electronic supplementary material, figure S1). The dashed and dotted lines represent the values of P_I for a gene of 1 and 10 kb (haplotype blocks in Eukaryotes range from 10 kb to hundreds of kb [47]), respectively, and a mutation rate of 10⁻⁸ bp⁻¹ (mutation rates in animals range from 10⁻⁹ bp⁻¹ to 5.10⁻⁸ bp⁻¹ [48]).