Warthog Genomes Resolve an Evolutionary Conundrum and Reveal Introgression of Disease Resistance Genes

Abstract

African wild pigs have a contentious evolutionary and biogeographic history. Until recently, desert warthog (Phacochoerus aethiopicus) and common warthog (P. africanus) were considered a single species. Molecular evidence surprisingly suggested they diverged at least 4.4 million years ago, and possibly outside of Africa. We sequenced the first whole-genomes of four desert warthogs and 35 common warthogs from throughout their range. We show that these two species diverged much later than previously estimated, 400,000–1,700,000 years ago depending on assumptions of gene flow. This brings it into agreement with the paleontological record. We found that the common warthog originated in western Africa and subsequently colonized eastern and southern Africa. During this range expansion, the common warthog interbred with the desert warthog, presumably in eastern Africa, underlining this region’s importance in African biogeography. We found that immune system–related genes may have adaptively introgressed into common warthogs, indicating that resistance to novel diseases was one of the most potent drivers of evolution as common warthogs expanded their range. Hence, we solve some of the key controversies surrounding warthog evolution and reveal a complex evolutionary history involving range expansion, introgression, and adaptation to new diseases.

African Suid Genomes Provide Insights into the Local Adaptation to Diverse African Environments

“…1 C ). This corresponds to the expansion of western populations of common warthog into eastern and then southern Africa from the start of the Late Pleistocene ( Garcia-Erill et al 2022 ). During the Last Glaciation, a cold arid climate prevailed with the fragmented forests as well as the expanded savannah-grassland areas in the tropical African belt ( Hamilton and Taylor 1991 ), whereas vegetation (shrubs and grassland) in the LGM covered markedly more areas on the land than today in the Sahara ( Shao et al 2018 ).…”

“…The success of extant African suids in various ecological niches indicates that they are excellent models to study the genetics of mammalian adaptive evolution in sub-Saharan Africa, which can provide additional valuable information on the spread of the family Suidae in Africa. Nevertheless, most of the previous studies associated with the extant African suids focused largely on phylogeny ( Gongora et al 2011 ; Liu et al 2019 ), phylogeography ( Muwanika et al 2003 ; Garcia-Erill et al 2022 ), social organization ( Muwanika et al 2007 ; White et al 2010 ), conservation biology ( Adeola et al 2021 ; Codjia et al 2021 ), feeding and reproductive biology ( Boshe 1981 ; Berger et al 2006 ; Edossa et al 2021 ), as well as infectious and parasitic diseases ( Luther et al 2007 ; Everett et al 2011 ; Blomstrom et al 2012 ; Apanaskevich et al 2013 ; Ebhodaghe et al 2021 ; Friant et al 2022 ). These have laid foundations for the preliminary understanding on their phylogeny, behavior, and adaptation.…”

“…These have laid foundations for the preliminary understanding on their phylogeny, behavior, and adaptation. With the accumulation of genomic data in recent years for the family Suidae ( Groenen et al 2012 ; Frantz et al 2013 , 2016 ; Groenen 2016 ; Liu et al 2019 , 2022 ; Warr et al 2020 ; Garcia-Erill et al 2022 ), this provides a baseline that will underpin further studies on the potential molecular mechanisms of the evolution and phenotypic adaptations of the African suids with genomic approaches.…”

Persistent gene flow suggests an absence of reproductive isolation in an African antelope speciation model

“…The levels of genetic diversity from Luangwa and Kafue are high compared to other large African mammals we have investigated, e.g. 0.00396 in Cape buffalo (Quinn et al in prep), 0.00207 in desert warthog and 0.00262 in common warthog 25 , and 0.00201 in African leopard 26 , and also higher than many other species of large mammal 27 . Additionally, heterozygosity distributions were almost entirely non-overlapping when considering adjoining populations, providing further support to consider each sampling location as genetically distinct populations.…”

An Updated Review of Ornithodoros Ticks as Reservoirs of African Swine Fever in Sub-Saharan Africa and Madagascar

“…East Africa can be considered the real cradle of ASFV. Indeed, based on molecular clock studies, warthog populations from the Horn of Africa ( Phacochoerus aethiopicus ) have been maintaining ASF genes for more than 1.4 million years [ 75 , 76 ]. In addition to the seminal paper by Montgomery [ 3 ] in which the disease was first described from Kenya, the confirmation that warthog-burrow-associated Ornithodoros ticks were vectors of the disease was first reported in three East African countries (Kenya, Tanzania, and Uganda) in the late 1960s and early 70s [ 5 , 7 , 8 , 49 ].…”