Integrating coalescent species delimitation with analysis of host specificity reveals extensive cryptic diversity despite minimal mitochondrial divergence in the malaria parasite genus Leucocytozoon.

BACKGROUND: Coalescent methods that use multi-locus sequence data are powerful tools for identifying putatively reproductively isolated lineages, though this approach has rarely been used for the study of microbial groups that are likely to harbor many unrecognized species. Among microbial symbionts, integrating genetic species delimitation methods with trait data that could indicate reproductive isolation, such as host specificity data, has rarely been used despite its potential to inform species limits. Here we test the ability of an integrative approach combining genetic and host specificity data to delimit species within the avian malaria parasite genus Leucocytozoon in central Alaska. RESULTS: We sequenced seven nuclear loci for 69 Leucocytozoon samples and used multiple species delimitation methods (GMYC and BPP models), tested for differences in host infection patterns among putative species based on 406 individual infections, and characterized parasite morphology. We found that cryptic morphology has masked a highly diverse Leucocytozoon assemblage, with most species delimitation methods recovering support for at least 21 separate species that occur sympatrically and have divergent host infection patterns. Reproductive isolation among putative species appears to have evolved despite low mtDNA divergence, and in one instance two Leucocytozoon cytb haplotypes that differed by a single base pair (~ 0.2% divergence) were supported as separate species. However, there was no consistent association between mtDNA divergence and species limits. Among cytb haplotypes that differed by one to three base pairs we observed idiosyncratic patterns of nuclear and ecological divergence, with cytb haplotype pairs found to be either conspecific, reproductively isolated with no divergence in host specificity, or reproductively isolated with divergent patterns of host specialization. CONCLUSION: Integrating multi-locus genetic species delimitation methods and non-traditional ecological data types such as host specificity provide a novel view of the diversity of avian malaria parasites that has been missed previously using morphology and mtDNA barcodes. Species delimitation methods show that Leucocytozoon is highly species-rich in Alaska, and the genus is likely to harbor extraordinary species-level diversity worldwide. Integrating genetic and ecological data will be an important approach for understanding the diversity and evolutionary history of microbial symbionts moving forward.

Hybridization of Atlantic puffins in the Arctic coincides with 20th-century climate change.

The Arctic is experiencing the fastest rates of global warming, leading to shifts in the distribution of its biota and increasing the potential for hybridization. However, genomic evidence of recent hybridization events in the Arctic remains unexpectedly rare. Here, we use whole-genome sequencing of contemporary and 122-year-old historical specimens to investigate the origin of an Arctic hybrid population of Atlantic puffins (Fratercula arctica) on Bjørnøya, Norway. We show that the hybridization between the High Arctic, large-bodied subspecies F. a. naumanni and the temperate, smaller-sized subspecies F. a. arctica began as recently as six generations ago due to an unexpected southward range expansion of F. a. naumanni. Moreover, we find a significant temporal loss of genetic diversity across Arctic and temperate puffin populations. Our observations provide compelling genomic evidence of the impacts of recent distributional shifts and loss of diversity in Arctic communities during the 20th century.