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. 2023 Dec 5;21(1):282.
doi: 10.1186/s12915-023-01771-3.

Diversity across organisational scale emerges through dispersal ability and speciation dynamics in tropical fish

Thomas Keggin  1   2 , Conor Waldock  3   4 , Alexander Skeels  5   6   7 , Oskar Hagen  8   9 , Camille Albouy  5   6 , Stéphanie Manel  10   11 , Loïc Pellissier  5   6
Affiliations

Diversity across organisational scale emerges through dispersal ability and speciation dynamics in tropical fish

Thomas Keggin et al. BMC Biol. .

Abstract

Background: Biodiversity exists at different levels of organisation: e.g. genetic, individual, population, species, and community. These levels of organisation all exist within the same system, with diversity patterns emerging across organisational scales through several key processes. Despite this inherent interconnectivity, observational studies reveal that diversity patterns across levels are not consistent and the underlying mechanisms for variable continuity in diversity across levels remain elusive. To investigate these mechanisms, we apply a spatially explicit simulation model to simulate the global diversification of tropical reef fishes at both the population and species levels through emergent population-level processes.

Results: We find significant relationships between the population and species levels of diversity which vary depending on both the measure of diversity and the spatial partitioning considered. In turn, these population-species relationships are driven by modelled biological trait parameters, especially the divergence threshold at which populations speciate.

Conclusions: To explain variation in multi-level diversity patterns, we propose a simple, yet novel, population-to-species diversity partitioning mechanism through speciation which disrupts continuous diversity patterns across organisational levels. We expect that in real-world systems this mechanism is driven by the molecular dynamics that determine genetic incompatibility, and therefore reproductive isolation between individuals. We put forward a framework in which the mechanisms underlying patterns of diversity across organisational levels are universal, and through this show how variable patterns of diversity can emerge through organisational scale.

Keywords: Dispersal; Ecology; Macroevolution; Models/simulations; Speciation; Species-genetic diversity correlations.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Simulated β- and γ-diversity relationships between the population and species levels of organisation across three measures of diversity; richness, phylogenetic diversity (PD), and mean pairwise distance (MPD). The grey dashed line represents a 1:1 positive relationship between the two levels, whilst the black solid lines represent the simulated relationship found through a significant (p < 0.05) simple linear regression. a All β-diversity relationships are positive, and b all but richness γ-diversity relationships are negative. Dark colours represent higher relative species diversity and lighter colours represent higher relative population diversity. All diversity measures have been log-transformed for both the regressions and visualisation. Figure data are available in Additional file 4
Fig. 2
Fig. 2
a Plots of multiple linear regression predictor coefficients showing the direction and magnitude of impact on population-species continuity metrics across each facet of diversity. Negative values (light blue) indicate that increasing the parameter value drives the relative diversity towards the population-level, whilst positive values (dark blue) drive diversity to the species-level. Horizontal bars represent the standard error. Greyed parameters are less significant (p > 0.05). b Scatterplot of continuity metrics against the most significant parameter, the speciation threshold. Positive values (dark blue) indicate relatively more species diversity and negative values (light blue) indicate relatively more population diversity. Figure data are available in Additional file 5
Fig. 3
Fig. 3
a Plot of the correlations between diversity continuity metrics and clade properties. Light blue indicates that increasing the clade property value is associated with an increased relative population-level diversity compared to species-level diversity, and vice versa for dark blue. Crosses indicate non-significant (p > 0.05) values. b-d PCA plots of each continuity metric and clade properties. Dark blue arrows indicate a significant (p < 0.05) correlation between the clade property and a relative increase in species-level to population-level diversity. Light blue indicates a significant correlation in the opposite direction. Grey clade properties had no significant relationship with the continuity metric. Figure data are available in Additional file 6
Fig. 4
Fig. 4
Conceptual diagram of the partitioning of diversity through speciation and the accumulation of divergence across levels of organisation. The species and population levels of organisation are represented by dark and light blue, respectively. a For richness, the total number of populations stays the same when speciation occurs, but another species is added to the system — 1 species and 4 populations becomes 2 species and 4 populations. This creates an uneven increase in the number of objects at each level. b Phylogenetic trees constructed from population objects are nested within species phylogenies. For phylogenetic diversity and mean pairwise distance, the phylogenetic tree topography, and therefore total diversity, is conserved throughout the speciation process. However, some of the population-level diversity is partitioned from the population-level to the species-level. Since speciation does not add or remove total diversity from the system, but rather transfers it directly from one to another, this dynamic drives a negative relationship between the species and population levels of diversity. c For divergence, (i) at the population-level the upper limit is determined by the speciation threshold and divergence is slowed by gene-flow and (ii) at the species-level there is no upper limit and few brakes inhibiting divergence between species over time. The dotted horizontal line represents a speciation event
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