Glasenapp MR and Pogson GH (2023), Extensive introgression among strongylocentroti...

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Ecol Evol 2023 Aug 25;138:e10446. doi: 10.1002/ece3.10446.

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Extensive introgression among strongylocentrotid sea urchins revealed by phylogenomics.

Glasenapp MR , Pogson GH .

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Gametic isolation is thought to play an important role in the evolution of reproductive isolation in broadcast-spawning marine invertebrates. However, it is unclear whether gametic isolation commonly evolves early in the speciation process or only accumulates after other reproductive barriers are already in place. It is also unknown whether gametic isolation is an effective barrier to introgression following speciation. Here, we used whole-genome sequencing data and multiple complementary phylogenomic approaches to test whether the well-documented gametic incompatibilities among the strongylocentrotid sea urchins have limited introgression. We quantified phylogenetic discordance, inferred reticulate phylogenetic networks, and applied the Δ statistic using gene tree topologies reconstructed from multiple sequence alignments of protein-coding single-copy orthologs. In addition, we conducted ABBA-BABA tests on genome-wide single nucleotide variants and reconstructed a phylogeny of mitochondrial genomes. Our results revealed strong mito-nuclear discordance and considerable nonrandom gene tree discordance that cannot be explained by incomplete lineage sorting alone. Eight of the nine species examined demonstrated a history of introgression with at least one other species or ancestral lineage, indicating that introgression was common during the diversification of the strongylocentrotid urchins. There was strong support for introgression between four extant species pairs (Strongylocentrotus pallidus ⇔ S. droebachiensis, S. intermedius ⇔ S. pallidus, S. purpuratus ⇔ S. fragilis, and Mesocentrotus franciscanus ⇔ Pseudocentrotus depressus) and additional evidence for introgression on internal branches of the phylogeny. Our results suggest that the existing gametic incompatibilities among the strongylocentrotid urchin species have not been a complete barrier to hybridization and introgression following speciation. Their continued divergence in the face of widespread introgression indicates that other reproductive isolating barriers likely exist and may have been more critical in establishing reproductive isolation early in speciation.

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	FIGURE 1. (a) Phylogeny of the nine strongylocentrotid sea urchin species included in the study. A maximum likelihood species tree was inferred using the edge‐linked partition model of IQ‐TREE (Chernomor et al., 2016; Nguyen et al., 2015) on 4497 concatenated single‐copy ortholog alignments. Branch supports were obtained using ultrafast bootstrap (Hoang et al., 2018) with 1000 replicates. Gene concordance factor (gCF) and site concordance factor (sCF) statistics (Minh et al., 2020; Mo et al., 2022) were calculated using IQ‐TREEv2.2.2. For each branch in the species tree, the gCF measures the proportion of gene trees containing that branch, while the sCF measures the proportion of informative sites concordant with that branch (Minh et al., 2020). (b) Extended output from the gene concordance factor statistics, showing the most frequent discordant topologies (df1, df2) for branches in the species tree with significant imbalances in the frequencies of df1 and df2. The frequencies of the df1 and df2 topologies are expected to be equal under incomplete lineage sorting alone. Species abbreviations: Sdro, S. droebachiensis; Sfra, S. fragilis; Spal, S. pallidus; Sint, S. intermedius; Spur, S. purpuratus; Hpul, H. pulcherrimus; Mnud, M. nudus; Mfra, M. franciscanus; Pdep, P. depressus.
	FIGURE 2. A maximum likelihood tree of mitochondrial genome assemblies was inferred from the same samples used in the nuclear species tree shown in Figure 1a. Both nuclear and mitochondrial trees were rooted at the midpoint. The mitochondrial genomes were aligned using Clustal Omega v1.2.3, and a maximum likelihood tree was constructed using IQ‐TREE (Nguyen et al., 2015) and ModelFinder (Kalyaanamoorthy et al., 2017). Branch supports were obtained using ultrafast bootstrap (Hoang et al., 2018) with 1000 replicates. Relative to the true species relationships (Figure 1a), the placements of the following are swapped: (i) M. nudus and P. depressus, (ii) S. purpuratus and S. intermedius, and (iii) S. pallidus and S. fragilis.
	FIGURE 3. Results of ABBA–BABA tests for all phylogenetically relevant triplets. Equal numbers of ABBA and BABA sites are expected under the null hypothesis of no introgression (D = 0). A positive D statistic indicates introgression between P3 and P2. Significance was assessed using a block jackknife size of 1 Mb. Error bars represent the standard error. Species abbreviations: Sdro, S. droebachiensis; Sfra, S. fragilis; Spal, S. pallidus; Sint, S. intermedius; Spur, S. purpuratus; Hpul, H. pulcherrimus; Mnud, M. nudus; Mfra, M. franciscanus; Pdep, P. depressus.
	FIGURE 4. Phylogenetic networks with reticulation edges and inheritance probabilities inferred by PhyloNet InferNetwork_ML. The inheritance probabilities represent the proportion of sampled genes inherited through gene flow. The network with zero reticulation edges recovered the species relationships and had a log‐likelihood of −11,054 (not shown). (a) The best network with one reticulation edge (log‐likelihood: −10,966). (b) The second‐best network with one reticulation edge (log‐likelihood: −10,976). (c) The network inferred with two reticulation edges (log likelihood: −10,929). (d) The network inferred with three reticulation edges (log‐likelihood: −10,903). Species abbreviations: Sdro, S. droebachiensis; Sfra, S. fragilis; Spal, S. pallidus; Sint, S. intermedius; Spur, S. purpuratus; Hpul, H. pulcherrimus; Mfra, M. franciscanus.

References [+] :

Addison, Multiple gene genealogies reveal asymmetrical hybridization and introgression among strongylocentrotid sea urchins. 2009, Pubmed, Echinobase