NREM/ZOOL 4464 – Ornithology Lectures 9–11 Dr. Tim O’Connell 4, 6, & 8 February 2019

Taxonomy redefined: systematics

Methods of systematics

•Phenetics – lumps organisms in categories based on degrees of overall similarity, with no attempt to reflect evolutionary history. Can be vulnerable to lumping species together based on analogous structure, e.g., beak similarities among species we now know are not close relatives. (This is essentially what Linnaeus did.)

•analogous structures develop through convergent evolution, i.e., similarity in form and function in response to similar selective pressure. Analogous structures do not indicate a common evolutionary origin.

For example, birds, bats, and pterosaurs are the only vertebrate groups that have powered flight, and all have evolved wings.

•Each group, however, evolved its wings independently: pterosaur wings were sheets of skin supported by one huge finger bone; bat wings are skin supported by enlarged hand bones; bird wings are feather surfaces supported by fused arm, hand, and finger bones.

•Note, however, that while their wings are analogous structures, their forelimbs are homologous structures. •Homologous structures indicate a common evolutionary origin, regardless of how similar the structures might appear. •The common ancestor of reptiles, birds, and mammals had a forearm comprised of humerus, radius and ulna, metacarpals, carpals, and phalanges that ended in a 5-toed foot. Those same bones (most of them at least) can be found in wings of birds, bats, and pterosaurs.

Example of potential confusion in taxonomy: •Finches have conical beaks that are good at cracking seeds. •Warblers have thin, pointed beaks that are good for collecting insects. •The Warbler Finch looks like a warbler, and collects insect food just like warblers do. The similarity, however, is due to convergence – this bird is a finch, descended from finches. Its “warbler” beak is a product of convergent evolution on warbler structure, not common ancestry with warblers.

Homologous versus Analogous structures become really important when trying to reconstruct phylogeny.

•Cladistics – weights the importance of some traits over others. Ancestral traits like “two legs” are not that useful for classifying within birds – they all have two legs. More important are shared, derived characters (“synapomorphies”) that indicate homologous structure. A cladistic approach strives for 100% objectivity in comparing numbers of synapomorphies among groups.

•Phenetics - DEGREE of divergence is paramount. Taxa are grouped by gross overall similarity (morphology) •Cladistics - TIME since divergence is paramount. It doesn’t matter what they look like overall, it’s evidence for ancestry that really counts (inferred genetics)

•The number of shared, derived characters (synapomorphies) is important in determining ancestry

1 •Ex) humans aren’t closely related to chimps because both species have hair and nurse their young [all mammals do that], but rather because both have 5-fingered hands with opposable thumbs, stereoscopic vision, big brains, no tails, bunodont dentition, etc. •It’s the things we have in common with chimps that we don’t have in common with other mammals that provide the most insight.

•All groups (“clades”) should be MONOPHYLETIC •Monophyletic group: all members are descended from a single common ancestor; all descendants of that ancestor are in the clade •Sounds silly, but this has huge implications for understanding what makes a bird, a bird.

Consider this phylogenetic tree, a cladogram. Species a is the common ancestor of species d, e, g, h, k, and l.

Taxon 1 is monophyletic: A single, common ancestor (b) gave rise to all species in the taxon with no descendants placed in any other taxon.

Ex) All bears are in the family Ursidae; there is nothing descended from bears that is in any other family.

Taxon 2 is polyphyletic: Members of this taxon are descendants of more than one common ancestor, in this case, both (c) and (f) are ancestral.

The kingdom Plantae is polyphyletic because flowering plants and mosses are both plants but they arose from different ancestors.

Taxon 3 is paraphyletic: In this case, the taxon excludes species that share a common ancestor with the one or more species in the taxon.

The Class Reptilia is paraphyletic because it does not include mammals or birds both of which are descended from reptiles.

2 Methods of Systematics •Phenetics – lumps organisms in categories based on degrees of overall similarity, with no attempt to reflect evolutionary history. •Cladistics – weights the importance of synapomorphies over other traits.

•Evolutionary systematics – weights homologous traits even further than cladistics, using the logic that some traits may be shared and derived but irrelevant to the life history. If the feature doesn’t play a key role in fitness, why use it for classification?

•Cladisitic revolution – biochemical genetics: directly compares the amount of genetic divergence between groups, i.e., the Holy Grail of systematics.

DNA/DNA hybridization

•DNA/DNA hybridization (from Fred Sheldon’s work on herons): •a = GTBH/GTBH, b = GTBH/GREG, c = GTBH/AMBI, d = GTBH/GLIB

Depending on what DNA source is used, hybridization and similar approaches can be used to illustrate relationships within a clade:

. . . Or they could illustrate everything from broad relationships among orders to actual genetic diversity within a single population. Here’s an example of the latter:

Required Reading:

Zink, R. M., A. W. Jones, C. C. Farquhar, M. C. Westberg, and J. I. Gonzalez Rojas. 2010. Comparison of molecular markers in the endangered Black-capped Vireo (Vireo atricapilla) and their interpretation in conservation. The Auk 127: 797–806.

•Collaborators: University of Minnesota, Cleveland Museum of Natural History, Texas Parks and Wildlife Department, Independent University of Nuevo Leon

•Lead author Bob Zink. Active in molecular systematics of birds for at least 25 years; a leader in exploring species concepts in evolutionary biology.

3 The Black-capped Vireo •Endemic songbird of oak scrub and savanna in the Southern Plains. •Loss of habitat (fire suppression, urbanization) and brood parasitism by Brown-headed Cowbird caused population decline in 20th Century and isolation of breeding occurrences. Bottomed out at < 200 pairs in U.S. by 1990s. •Now nests only in northern Mexico (two states there), central Texas, and southwestern Oklahoma. (Winters in southwestern Mexico.) •Listed as “endangered” in U.S. and Mexico, “vulnerable” by IUCN. Now about 1000 pairs in OK. •Conservation genetics issue: if breeding occurrences are isolated from each other, does this mean that gene flow is restricted? •Gene flow – transfer of alleles from one population to another. Gene flow is restricted in allopatric (“other country”) populations (those separated by some barrier) and generally prevalent in sympatric populations.

Reduced gene flow in allopatric populations considered first step toward reproductive isolation, i.e., speciation or extinction.

Isolated occurrences of Black-capped Vireo: •If gene flow is restricted, this could lead to genetic bottlenecks in separate occurrences. •Genetic bottleneck – event leading to significant reduction in genetic diversity within a population. Reduced diversity can result in inbreeding and inability to respond to new selective pressures.

Conservation Genetics: How do we examine the degree of genetic diversity in a population? •Genes are sequences of nucleotide base pairs at specific locations in a DNA strand that code for some trait, e.g., eye color or the production of an enzyme. •Alleles are different forms of genes, e.g., blue eyes vs. brown eyes or variable structures of an enzyme that still catalyzes the same reaction. •Polymorphism – two or more discrete phenotypes in a sympatric population. Examples include tan-striped and white-striped White-throated Sparrows, human blood types, etc.

Examine source of polymorphisms! Three examples: 1. Alloenzymes – generally conservative (low mutation rate) so polymorphisms can be strong indicator of evolutionary change. 2. Microsatellites – repeated sequences of 1–6 base pairs of DNA. High mutation rates result in lots of polymorphisms – in other words, there are lots of different alleles to examine in a microsatellite. These can indicate genetic diversity within populations of the same species. 3.Mitochondrial DNA – yep, mitochondria have their own DNA – can also serve as useful genetic markers, but limited by the size of the genome and only inherited from the maternal line. Can distinguish among individuals.

Zink et al. 2010: Introduction – •Some authors questioning the use of mitochondrial DNA (mtDNA) •Zink has data to suggest that for birds it matches up well with similar studies of nuclear DNA (e.g., microsatellites). •If anything, microsatellites might be unreliable for some applications because they mutate so frequently. •Goal: “analysis of molecular variance” or AMOVA – to identify differences within populations that have been isolated. a.k.a. “genetic structure” •In this case, use Black-capped Vireo as a model to test mtDNA vs. microsatellites in AMOVA

4 •Previous study of allozymes showed differentiation of the Oklahoma population – will new analysis using microsatellites and mtDNA confirm this?

Methods – •Obtained feathers from birds in OK, TX, and Mexico (n = 108) • Extracted DNA from feathers and ran analysis on DNA

Results - •From mtDNA, only 2 of 9 analyses showed divergence. •On balance, no evidence for genetic structuring

•From microsatellites, more evidence for structuring: “isolation by distance”, but only for about 2.4% of the molecular variance. •In other words, 98% of the variance not explained by geography.

Discussion - •From microsatellites and mtDNA, <3% of genetic variation explained by location = low evidence of genetic structuring. •Previous studies demonstrating genetic structure using more restricted data have concluded that emphasis in conservation shift to promoting dispersal among populations. •Zink et al. conclude that dispersal is happening without human intervention. •Statistical significance in conservation genetics does not necessarily lead to biological significance for conservation.

•Thus, no need to establish corridors to “link” the disjunct populations. Despite the distances between the separate occurrences, gene flow is taking place.

Okay, so what about relationships at really broad levels?

Modern hierarchy of life on earth: •Species (plural “species”) •Domain •Kingdom •Phylum (plural “phyla”) •Class •Order Within Animalia •Family •Phylum Chordata •Genus (plural “genera”) •Subphylum Vertebrata •Class Aves

Among birds, one big and obvious anatomical split has been the structure of the body palate of the upper mandible. The more ancestral condition (“paleognath”) is found in ostriches, emus, kiwis, elephant birds, moas, rheas, and the chicken-like tinamous. All other modern bird species (like nearly 10,000 species) share a more derived palate structure (“neognath”).

From Gussekloo et al. 2017: palate structure in paleognaths, neognaths, and Archaeopteryx. There are at least 7 differences in palates between paleo- and neognaths (Archaeopteryx in between). For example, the maxilla (yellow) was big in Archaeopteryx and is big in paleognaths but it much reduced in neognaths.

5 That’s fine, but do we really have enough anatomical differences to understand the evolutionary relationships among the Aves? Toe arrangement, feather structure, natal development – these traditional comparative approaches have provided a basic understanding of relationships, but those relationships have in some cases been called into question by DNA-DNA hybridization studies, notably that of Sibley and Ahlquist in 1990. That just begs the question: how do we know that Sibley and Ahlquist did any better?

Our best opportunity to solve the problem would be to compare entire avian genomes . . .

The Avian Phylogenetics Consortium recently published a series of papers that confirm some long-held suspicions about avian systematics, and provide some surprises too.

More than 200 scientists at 80 research institutions have contributed to this colossal study in which the whole genomes of 48 species were analyzed and compared. Those species represented all 32 Neognath orders and 2 (of the 5) Paleognath orders for the most complete picture of avian phylogenetics yet.

The results look a bit like this:

The big splits –

Aves Paleognathae – ostriches, emus, tinamous, etc. Neognathae – everything else

Neognathae Galloanseres – chickeny and ducky things Neoaves – everything else

Neoaves Columbea – pigeony things (includes grebes and flamingoes!) Passerea – everything else

Passerea The remaining 22 orders of birds, mostly falling along traditional lines of taxonomy

6 To begin to get you comfortable in thinking about orders and families of birds, here are some plates from the Handbook of the Birds of the World:

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