Parallel evolution of integrated craniofacial traits in trophic specialist pupfishes

Author:

St. John Michelle E.1,Dunker Julia C.2,Richards Emilie J.3,Romero Stephanie4,Martin Christopher H.25ORCID

Affiliation:

1. Department of Biology University of Oklahoma Norman Oklahoma USA

2. Department of Integrative Biology University of California Berkeley California USA

3. Department of Ecology, Evolution and Behavior University of Minnesota Minneapolis Minnesota USA

4. Department of Evolution and Ecology University of California Davis California USA

5. Museum of Vertebrate Zoology University of California Berkeley California USA

Abstract

AbstractPopulations may adapt to similar environments via parallel or non‐parallel genetic changes, but the frequency of these alternative mechanisms and underlying contributing factors are still poorly understood outside model systems. We used QTL mapping to investigate the genetic basis of highly divergent craniofacial traits between the scale‐eater (Cyprinodon desquamator) and molluscivore (C. brontotheroides) pupfish adapting to two different hypersaline lake environments on San Salvador Island, Bahamas. We lab‐reared F2 scale‐eater x molluscivore intercrosses from two different lake populations, estimated linkage maps, scanned for significant QTL for 29 skeletal and craniofacial traits, female mate preference, and sex. We compared the location of QTL between lakes to quantify parallel and non‐parallel genetic changes. We detected significant QTL for six craniofacial traits in at least one lake. However, nearly all shared QTL loci were associated with a different craniofacial trait within each lake. Therefore, our estimate of parallel evolution of craniofacial genetic architecture could range from one out of six identical trait QTL (low parallelism) to five out of six integrated trait QTL (high parallelism). We suggest that pleiotropy and trait integration can affect estimates of parallel evolution, particularly within rapid radiations. We also observed increased adaptive introgression in shared QTL regions, suggesting that gene flow contributed to parallel evolution. Overall, our results suggest that the same genomic regions may contribute to parallel adaptation across integrated suites of craniofacial traits, rather than specific traits, and highlight the need for a more expansive definition of parallel evolution.

Funder

National Institute of Dental and Craniofacial Research

Division of Environmental Biology

Publisher

Wiley

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