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Unravelling the geographic structure and introgressive spread of a sexually selected colour ornament in wall lizards (Podarcis muralis)

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posted on 2023-11-02, 00:36 authored by Maravillas Ruiz MinanoMaravillas Ruiz Minano

Species can display fascinating and sometimes extreme phenotypic diversity across their geographical range. One of the possible explanations for this variation is the dynamic nature of selection pressures across different environments. In particular, climate is an important environmental factor which has been shown to mediate the strength of both natural and sexual selection and thus contribute to patterns of phenotypic diversity across the landscape. However, selection is not the only process that contributes to phenotypic diversity. Instead, the variation observed today is the result of several processes including historical changes in the distribution of populations, contemporary gene flow as well as ongoing selection. Teasing apart the mechanisms underlying the evolution of phenotypic variation remains a challenge.
Wall lizards (genus Podarcis) are well-known for their extraordinary phenotypic variation across their distribution. One good example is the distribution of colour ornaments in common wall lizards (Podarcis muralis) in Italy. Males from certain parts of central Italy exhibit exaggerated colour ornamentation, including bright green dorsal colouration and extensive black ventral colouration. This colouration is accompanied by a large body and head size, strong bite force, and dominant behaviour. Previous research suggests that this colour ornamentation originated in the south-west of Italy, and then spread northward under sexual selection, eventually introgressing into a distantly related lineage (the Southern Alps lineage). Despite the strong and persistent spread of colouration, considerable variation in colour traits has been maintained both within and between lineages. In this thesis I take advantage of the expression of these exaggerated sexual traits within the Italian lineage, and its introgression into the Southern Alps lineage, to investigate the causes underpinning the colour variation we observe across the Italian landscape.
In the first chapter of my thesis, I tested if the geographic distribution of colour ornamentation can be explained by climate. Lizards are ectotherms and, as a result, climate is expected to strongly shape activity, social interactions and resource utilization and through this the strength of sexual selection. To test this, I applied a spatial analytical approach to data collected on wall lizard colour ornamentation from 114 populations across Italy, I found that colouration is highly structured across the landscape in a way that does not reflect broad-scale population genetic differentiation. Colour ornamentation is consistently exaggerated in environments characterized by a long annual reproductive season and reproductive season and consistently warm to hot thermal conditions during spring and summer. This is true both in terms of climate explaining variation in colouration observed within the Italian lineage as well as the introgressive spread of colouration into the Southern Alps lineage. Combined, this suggests that climate-driven selection may maintain geographic variation despite considerable gene flow between populations.
The spatial patterns of phenotypic variation in colouration identified in the first chapter of my thesis could be further intensified if colouration is associated, pleiotropically, with other key traits, specifically thermal physiology. Such pleiotropy, if antagonistic, may further restrict the movement of colour ornamentation into cool climates. In the second chapter of my thesis, I integrated a detailed field study of variation in microhabitat use between colour phenotypes with lab-based quantification of differences in thermal physiology to test this idea. I found that lizards with different degrees of ornamentation did not occupy different microhabitats nor did they maintain different field body temperatures. These results were corroborated by laboratory experiments, which demonstrated that lizards with different degrees of ornamentation had similar thermophysioloy, measured as preferred body temperature, critical thermal minimun, and temperature-dependent metabolic rate. Combined these data provide limited support for the hypothesis that pleiotropic links between colouration and thermophysiology are contributing to the climatically mediated distribution of colouration across the landscape.
In the final chapter of the thesis, I adopted a landscape genetics approach to investigate finescale genetic differentiation within the Italian lineage, and to test if climate consistently sorts specific alleles across the landscape (local adaptation). Using an extensive set of genomewide single nucleotide polymorphisms (SNPs), I revealed that climate explained a small, but statistically significant, amount of population genetic variation across the landscape. Given the overall low population genetic differentiation, these results support evidence for the strong and persistent climate-driven selection identified in Chapter 1. These findings were further supported by outlier detection analyses which identified several genes involved in metabolic and catabolic processes that may play an important role in thermal adaptation, that were linked to climatic predictors.
Combined, this thesis provides evidence for the importance of climate in modulating the strength of sexual selection across the geographic range of a species, that climate-driven sexual selection promotes introgression of sexual ornamentation. In addition, this thesis showed that climate is an important diver of local adaptation even in the face of gene. The high phenotypic variation observed in populations occupying intermediate climates may reflect the balance between selection and gene flow in this abundant species. Further studies are needed to (1) better understand how climate is modulating phenotypic and genetic structure, (2) fully test the contribution of small-scale spatial heterogeneity and variable environmental conditions between years and (3) expand genomic analyses using whole genome sequencing and gene function analyses.

History

Sub-type

  • PhD Thesis

Pagination

xv, 244 pages

Department/School

School of Natural Sciences

Publisher

University of Tasmania

Publication status

  • Unpublished

Event title

Graduation

Date of Event (Start Date)

2022-05-03

Rights statement

Copyright 2021 the author. Chapter 2 appears to be the equivalent of a pre-print version of an article published as: Ruiz Minano, M., While, G. M., Yang, W., Burridge, C. P., Sacchi, R., Zuffi, M., Scali, S., Salvi, D., Uller, T., 2021, Climate shapes the geographic distribution and introgressive spread of color ornamentation in common wall lizards, American naturalist, 198(3), 379-393.

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