Modern ecology explains ancient population structure in a human-dominated landscape

Background/Question/Methods

Human domination has dramatically altered the ecological and evolutionary dynamics of life on Earth. While many species are ill equipped to survive human impacts, others persist and even thrive amidst anthropogenic change. Clearly the current ecologies of these two species groups differ, but how did attributes that today permit species to survive in human-modified habitats influence their ecologies prior to recent anthropogenic change? We explore this question by comparing the demographic history and population connectivity of two species of neotropical leaf litter frogs with contrasting habitat affiliations in a human-dominated landscape. Both Craugastor crassidigitus (restricted to native forest habitats) and C. fitzingeri (human affiliated) are native to the study area in southern Costa Rica, broadly similar ecologically, and closely related phylogenetically. The study region was largely covered by tropical moist forest until the mid-20^th century, when much of the native habitat was converted to agricultural lands. Specifically, we asked: i) What were the relative population sizes of these two species before widespread human modification of the landscape? ii) How were ancient populations structured spatially? and iii) How has recent agricultural expansion altered population structure?

Results/Conclusions

We sequenced 783 bp of mitochondrial cytochrome b from a total of 529 individuals of both species across the landscape. In addition to revealing recent demographic change, we uncovered patterns of older demographic history.  We recovered 20 unique haplotypes in the forest-restricted C. crassidigitus, all of which are closely related and of recent origin, signaling population expansion over recent evolutionary time. However, smaller forest fragments possessed fewer haplotypes, signaling that genetic drift is already altering evolutionary dynamics after 60 years of land conversion. In contrast, our sample of the human-affiliated C. fitzingeri possesses only 10 haplotypes, segregated spatially across the landscape into two distantly related groups. Such partitioning indicates ancient barriers to dispersal—barriers not experienced by the forest-restricted species. Ecologically, these results suggest that C. fitzingeri originally existed at low population density, perhaps occupying forest gaps. Its population has expanded subsequent to human modification. Meanwhile, land conversion to agriculture has fragmented previously contiguous C. crassidigitus populations. Thus, depending on individual species’ life history, anthropogenic modification can either disrupt or enhance population connectivity. Such landscape conversion can lead to small populations at risk of inbreeding depression, or newly connected populations exchanging genes between anciently diverged lineages, with unpredictable microevolutionary consequences.