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Lemur Catta) in South-Central Madagascar Genetic consequences of occupying a highly fragmented landscape among ring-tailed lemurs (Lemur catta) in south-central Madagascar by Tara Anne Clarke MA, New Mexico State University, 2009 BA, Stony Brook University, 2005 A Dissertation Submitted in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY in the Department of Anthropology Tara Anne Clarke, 2015 University of Victoria All rights reserved. This dissertation may not be reproduced in whole or in part, by photocopy or other means, without the permission of the author. ii Supervisory Committee Genetic consequences of occupying a highly fragmented landscape among ring-tailed lemurs (Lemur catta) in south-central Madagascar by Tara Anne Clarke MA, New Mexico State University, 2009 BA, Stony Brook University, 2005 Supervisory Committee Dr. Lisa Gould, Department of Anthropology Supervisor Dr. Helen Kurki, Department of Anthropology Departmental Member Dr. Joyce A. Parga, Department of Anthropology, California State University, Los Angeles Non-Unit Member iii Abstract Supervisory Committee Dr. Lisa Gould, Department of Anthropology Supervisor Dr. Helen Kurki, Department of Anthropology Departmental Member Dr. Joyce A. Parga, Department of Anthropology Non-Unit Member Global climate change and habitat fragmentation represent two of the greatest threats to biodiversity and ecological processes worldwide. It is predicted that anthropogenic induced climate change could represent a key factor for extinctions in the near future, considering that the Earth is set to become warmer than at any period in the past 40 million years. Habitat fragmentation and isolation pose a number of challenges for the fauna inhabiting degraded areas, including lack of dispersal opportunities leading to inbreeding resulting in a loss of genetic diversity, reduced reproductive fitness; increases in vulnerability to predation, hunting, and disease, and an inability to deal with or respond to environmental changes and/or disease. Madagascar, the fourth largest island in the world, is home to unprecedented levels of endemism, including over 100 species of lemur. The island has undergone a range of historical and contemporary landscape transformations, both natural and anthropogenic. These landscape transformations combined with additional human- induced disturbances, such as the illegal pet and bushmeat trades, have had devastating effects on the island’s extant primate populations. Thus, Madagascar’s lemurs have been deemed the most endangered group of mammals and now represent the highest primate conservation priority in the world. The ring-tailed lemur (Lemur catta) is endemic to the southern regions of the island and occupies an array of habitats. L. catta is known for its remarkable behavioral and ecological flexibility, which contributes to its ability to exist in a mostly fragmented landscape. While this species represents one of the most well studied Malagasy strepsirhines, there has been a paucity of research regarding the population and conservation genetics of this endangered species. The goal of my dissertation was to iv examine the influence of habitat fragmentation and isolation on the genetic diversity and population structuring of this flagship species in three populations living in the central highlands of Madagascar: Anja Reserve, Sakaviro, and Tsaranoro Valley. Non-invasive fecal samples from 30 individual lemurs were collected from three fragmented forests and genotyped at six polymorphic microsatellite loci. Population genetic analyses were examined via GenAlEx software and revealed a moderate level genetic diversity. Genetic differentiation (FST) among the three fragmented populations ranged from 0.05-0.11. These data suggest that the L. catta populations within south-central Madagascar have not yet lost significant genetic variation. To examine past and recent demographic declines or genetic bottlenecks, I employed three approaches, including mode-shift and M-Ratio tests, as well as a test to detect heterozygosity excess using three mutation models: the two-phase model (TPM), step-wise mutation model (SMM), and the infinite allele model (IAM). Results were equivocal depending on the test that was applied; however, a mode-shift was detected for Anja, signifying this population underwent a historical bottleneck. M-ratio tests revealed that all three populations suffered historical bottlenecks. A population bottleneck was indicated via heterozygosity excess under the IAM for both the Anja and Sakaviro populations. To understand the impact of natural (e.g., mountains) and anthropogenic disturbances (e.g., roads, habitat fragmentation) on male reproductive strategies (dispersal) and population structuring, I utilized both GenAlEx and STRUCTURE software. Population assignment analyses suffered from a likely ‘lack of signal’. Therefore, individuals were unable to be reliably assigned to their population of origin. Genetic population structure was ambiguous. These data suggest that that these three fragmented populations are not genetically differentiated enough for proper population assignment, or perhaps the sample is not robust enough for population assignment analyses to produce unequivocal results. My research represents the first population genetic data for ring-tailed lemurs within the central highlands, and thus, serves as a baseline for future investigations into the genetic health of these populations. These data support the suggestion that these three v fragments represent areas in which concerted conservation efforts are necessary if genetic diversity is to be maintained and future demographic declines are to be prevented. My results are informative for the local community conservation associations working within south-central Madagascar and can now be applied to determine areas of conservation priority and where forest corridors will be the most beneficial for maintaining gene flow. The loss and fragmentation of habitat continues across Madagascar, including the central highlands; thus, all remaining L. catta populations should be considered a high conservation priority. If we are to safeguard the long-term viability of this species, continued conservation and research initiatives will be crucial. vi Table of Contents Supervisory Committee ...................................................................................................... ii Abstract .............................................................................................................................. iii Table of Contents ............................................................................................................... vi List of Tables ................................................................................................................... viii List of Figures .................................................................................................................... ix Acknowledgments............................................................................................................... x Dedication ........................................................................................................................ xiv Chapter 1. Introduction .................................................................................................... 1 1.1. Project Introduction .............................................................................................. 1 1.2. Microsatellite Markers: Challenges and Solutions ............................................... 2 1.3. Literature Cited ..................................................................................................... 5 Chapter 2. Background .................................................................................................... 9 2.1. Background ........................................................................................................... 9 2.1.1. Rafting Versus Land-Bridges: How Did Ancestral Lemurs Colonize Madagascar? ............................................................................................................. 10 2.1.2. Holocene Exinctions: What Happened To The Malagasy Megafauna? ...... 11 2.1.3. Contemporary Madagascar: Forest Fragments, Lemurs, And Conservation14 2.2. Background of Study Species ............................................................................. 18 2.2.1. Social Organization ...................................................................................... 18 2.2.2. Habitat Types and Geographic Range ......................................................... 20 2.2.3. Population Density and Home Range Size .................................................. 21 2.2.4. Diet and Feeding Ecology ............................................................................ 24 2.3. Study Sites .......................................................................................................... 25 2.4. Literature Cited ................................................................................................... 29 Chapter 3. Genetic Variability of Lemur catta in South-Central Madagascar .............. 41 3.1. Abstract ............................................................................................................... 41 3.2. Introduction ......................................................................................................... 42 3.3. Methods..............................................................................................................
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