Assessing the evolutionary persistence of ecological relationships: A review and preview

Abstract

Species interactions, such as pollination, parasitism and predation, form the basis of functioning ecosystems. The origins and resilience of such interactions therefore merit attention. However, fossils only occasionally document ancient interactions, and phylogenetic methods are blind to recent interactions. Is there some other way to track shared species experiences? "Comparative demography" examines when pairs of species jointly thrived or declined. By forging links between ecology, epidemiology, and evolutionary biology, this method sheds light on biological adaptation, species resilience, and ecosystem health. Here, we describe how this method works, discuss examples, and suggest future directions in hopes of inspiring interest, imitators, and critics.

Keywords: PSMC; anthropocene; bottleneck; comparative demography; ecology; effective population size; evolution; history; parasitism; pollination; population.

Graphical abstract

Fig. 1

Comparative demography seeks to infer whether, and when, distinct species have undergone shared intervals of population growth and contraction. Here, temporal changes in the estimated effective population size of each of two hypothetical species is illustrated. Note that the abundance of each species grew and contracted in concert over one temporal interval (to the left of the vertical dashed line; =) but at another interval, one species grew as the other contracted (to the right; ≠).

Fig. 2

Changes in population size influence when alleles coalesce. A. Here, the expected temporal distribution of branching in a population of constant size (above, orange) is contrasted with that expected for a population that has undergone a bottleneck (below, blue) (after Eriksson et al., 2010). In the constant-sized population, fewer coalescences are ascribed to the interval represented by the grey shading. B. The age of alleles diminishes exponentially in populations of constant size, but bottlenecks accelerate allelic loss, temporally concentrating coalescence events. C. Therefore, intervals of notably frequent coalescence events may demarcate periods of past population decline. Similar reasoning underlies procedures used to identify periods of population growth. Other factors (selection, population subdivision) may similarly influence such temporal patterns.

Fig. 3

A single diploid genome can be harnessed to estimate the age distribution of maternal and paternal alleles. Blocks of the genome are characterized by their heterozygote density, which is assumed to reflect for how long they have been accumulating differences.

Fig. 4

Inferring historical demography from the genomic distribution of heterozygosity. A. In a genomic walk, loci are categorized according to the density of heterozygous positions (for illustration purposes, depicted according to the accompanying heatmap where the darkest loci harbor the greatest density of heterozygous positions). B. A frequency distribution summarizes the proportion maternal and paternal alleles differing by few or many heterozygous positions. Loci distinguished by few heterozygotes are assumed to have diverged more recently than loci distinguished by many heterozygotes. C. Population decline favors allelic loss, whereas population growth favors allelic persistence. Adjusted for statistical expectations (which assume that most alleles in any given population are young), past population size estimates (red line) are inversely related to the age distribution of alleles in the genome (black histogram).

Fig. 5

Each segment of a temporally aligned pair of demographic history curves (A) is scored based on whether the population is growing, declining, or unchanged over that period (B). The residual differences in slope direction identifies periods of consistent or inconsistent population dynamics and summarize the overall fit between the pair of demographic history curves (C).

Fig. 6

The demographic histories of the malaria parasite (Plasmodium falciparum) and its mosquito vector (Anopheles gambiae) mirror human population growth; especially their increase in the last 10,000 years. Based on Hecht (2018) Fig. 1a. Effective population size is shown relative to each species’ average over the period.